Skip to main content
SpringerLink
Log in

The Evolving Role of Animal Models in the Discovery and Development of Novel Treatments for Psychiatric Disorders

  • Chapter
  • First Online:
Drug Development in Psychiatry

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 30))

  • 705 Accesses

Abstract

Historically, animal models have been routinely used in the characterization of novel chemical entities (NCEs) for various psychiatric disorders. Animal models have been essential in the in vivo validation of novel drug targets, establishment of lead compound pharmacokinetic to pharmacodynamic relationships, optimization of lead compounds through preclinical candidate selection, and development of translational measures of target occupancy and functional target engagement. Yet, with decades of multiple NCE failures in Phase II and III efficacy trials for different psychiatric disorders, the utility and value of animal models in the drug discovery process have come under intense scrutiny along with the widespread withdrawal of the pharmaceutical industry from psychiatric drug discovery. More recently, the development and utilization of animal models for the discovery of psychiatric NCEs has undergone a dynamic evolution with the application of the Research Domain Criteria (RDoC) framework for better design of preclinical to clinical translational studies combined with innovative genetic, neural circuitry-based, and automated testing technologies. In this chapter, the authors will discuss this evolving role of animal models for improving the different stages of the discovery and development in the identification of next generation treatments for psychiatric disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Patel V, Saxena S, Lund C, Thornicroft G, Baingana F, Bolton P, et al. The lancet commission on global mental health and sustainable development. Lancet. 2018;392:1553–98.

    Article  PubMed  Google Scholar 

  2. Center for Behavioral Health Statistics and Quality SA and MHS Administration. Substance Abuse and Mental Health Services Administration. Key substance use and mental health indicators in the United States: results from the 2020 National Survey on Drug Use and Health. Rockville, MD: Center for Behavioral Health Statistics and Quality SA and MHS Administration; 2020.

    Google Scholar 

  3. Lieberman JA, Stroup TS, McEvoy JP, Swartz MS, Rosenheck RA, Perkins DO, et al. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N Engl J Med. 2005;353:1209–23.

    Article  CAS  PubMed  Google Scholar 

  4. Fava M, Rush AJ, Trivedi MH, Nierenberg AA, Thase ME, Sackeim HA, et al. Background and rationale for the sequenced treatment alternatives to relieve depression (STAR*D) study. Psychiatr Clin North Am. 2003;26:457–94.

    Article  PubMed  Google Scholar 

  5. Rush AJ, Trivedi MH, Wisniewski SR, Nierenberg AA, Stewart JW, Warden D, et al. Acute and longer-term outcomes in depressed outpatients requiring one or several treatment steps: a STAR*D report. Am J Psychiatry. 2006;163:1905–17.

    Article  PubMed  Google Scholar 

  6. Watts BV, Schnurr PP, Mayo L, Young-Xu Y, Weeks WB, Friedman MJ. Meta-analysis of the efficacy of treatments for posttraumatic stress disorder. J Clin Psychiatry. 2013;74:11710.

    Article  Google Scholar 

  7. Garakani A, Murrough JW, Freire RC, Thom RP, Larkin K, Buono FD, et al. Pharmacotherapy of anxiety disorders: current and emerging treatment options. Front Psychiatry. 2020;11:595584.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Douaihy AB, Kelly TM, Sullivan C. Medications for substance use disorders. Soc Work Public Health. 2013;28:264–78.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Lindsley CW. New statistics on the cost of new drug development and the trouble with CNS drugs. ACS Chem Neurosci. 2014;5:1142.

    Article  CAS  PubMed  Google Scholar 

  10. Gribkoff VK, Kaczmarek LK. The need for new approaches in CNS drug discovery: why drugs have failed, and what can be done to improve outcomes. Neuropharmacology. 2017;120:11–9.

    Article  CAS  PubMed  Google Scholar 

  11. Hay M, Thomas DW, Craighead JL, Economides C, Rosenthal J. Clinical development success rates for investigational drugs. Nat Biotechnol. 2014;32:40–51.

    Article  CAS  PubMed  Google Scholar 

  12. Nestler EJ, Hyman SE. Animal models of neuropsychiatric disorders. Nat Neurosci. 2010;13:1161–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tricklebank MD, Robbins TW, Simmons C, Wong EHF. Time to re-engage psychiatric drug discovery by strengthening confidence in preclinical psychopharmacology. Psychopharmacology. 2021;238:1417–36.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Monteggia LM, Heimer H, Nestler EJ. Meeting report: can we make animal models of human mental illness? Biol Psychiatry. 2018;84:542–5.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Carretero M, Solis GM, Petrascheck M. C. elegans as model for drug discovery. Curr Top Med Chem. 2017;17:2067–76.

    Article  CAS  PubMed  Google Scholar 

  16. Artal-Sanz M, de Jong L, Tavernarakis N. Caenorhabditis elegans: a versatile platform for drug discovery. Biotechnol J. 2006;1:1405–18.

    Article  CAS  PubMed  Google Scholar 

  17. Fernández-Hernández I, Scheenaard E, Pollarolo G, Gonzalez C. The translational relevance of drosophila in drug discovery. EMBO Rep. 2016;17:471–2.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Patton EE, Zon LI, Langenau DM. Zebrafish disease models in drug discovery: from preclinical modelling to clinical trials. Nat Rev Drug Discov. 2021;20(8):611–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Bruni G, Lakhani P, Kokel D. Discovering novel neuroactive drugs through high-throughput behavior-based chemical screening in the zebrafish. Front Pharmacol. 2014;5:153.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Prior H, Haworth R, Labram B, Roberts R, Wolfreys A, Sewell F. Justification for species selection for pharmaceutical toxicity studies. Toxicol Res. 2021;9:758–70.

    Article  Google Scholar 

  21. Kaiser T, Feng G. Modeling psychiatric disorders for developing effective treatments. Nat Med. 2015;21:979–88.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Baker M, Hong SI, Kang S, Choi DS. Rodent models for psychiatric disorders: problems and promises. Lab Anim Res. 2020;36:1–10.

    Article  Google Scholar 

  23. Russel WMS, Burch RL. The principles of humane experimental technique. London: Meuthen; 1959.

    Google Scholar 

  24. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatr. 2003;160:636–45.

    Article  PubMed  Google Scholar 

  25. Willner P. The validity of animal models of depression. Psychopharmacology. 1984;83:1–16.

    Article  CAS  PubMed  Google Scholar 

  26. Green T, Gothelf D, Glaser B, Debbane M, Frisch A, Kotler M, et al. Psychiatric disorders and intellectual functioning throughout development in velocardiofacial (22q11.2 deletion) syndrome. J Am Acad Child Adolesc Psychiatry. 2009;48:1060–8.

    Article  PubMed  Google Scholar 

  27. Karayiorgou M, Simon TJ, Gogos JA. 22q11.2 microdeletions: linking DNA structural variation to brain dysfunction and schizophrenia. Nat Rev Neurosci. 2010;11(6):402–16.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Swerdlow NR, Braff DL, Taaid N, Geyer MA. Assessing the validity of an animal model of deficient sensorimotor gating in schizophrenic patients. Arch Gen Psychiatry. 1994;51:139.

    Article  CAS  PubMed  Google Scholar 

  29. Geyer MA, Krebs-Thomson K, Braff DL, Swerdlow NR. Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology (Berl). 2001;156(2-3):117–54.

    Article  CAS  PubMed  Google Scholar 

  30. Yankelevitch-Yahav R, Franko M, Huly A, Doron R. The forced swim test as a model of depressive-like behavior. J Vis Exp. 2015;(97):52587.

    Google Scholar 

  31. Sunal R, Gümüşel B, Kayaalp SO. Effect of changes in swimming area on results of “behavioral despair test”. Pharmacol Biochem Behav. 1994;49:891–6.

    Article  CAS  PubMed  Google Scholar 

  32. Geschwind DH, Flint J. Genetics and genomics of psychiatric disease. Science. 1979;2015(349):1489–94.

    Google Scholar 

  33. Rees E, Owen MJ. Translating insights from neuropsychiatric genetics and genomics for precision psychiatry. Genome Med. 2020;12(1):1–16.

    Article  Google Scholar 

  34. Anderzhanova E, Kirmeier T, Wotjak CT. Animal models in psychiatric research: the RDoC system as a new framework for endophenotype-oriented translational neuroscience. Neurobiol Stress. 2017;7:47–56.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Walters JTR, Owen MJ. Endophenotypes in psychiatric genetics. Mol Psychiatry. 2007;12:886–90.

    Article  CAS  PubMed  Google Scholar 

  36. Houdebine LM. Transgenic animal models in biomedical research. Methods Mol Biol. 2007;360:163–202.

    CAS  PubMed  Google Scholar 

  37. Skarnes WC, Rosen B, West AP, Koutsourakis M, Bushell W, Iyer V, et al. A conditional knockout resource for the genome-wide study of mouse gene function. Nature. 2011;474:337–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Ansorge MS, Zhou M, Lira A, Hen R, Gingrich JA. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science. 1979;2004(306):879–81.

    Google Scholar 

  39. Gordon JW, Scangos GA, Plotkin DJ, Barbosa JA, Ruddle FH. Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci. 1980;77:7380–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Nagy A. Cre recombinase: the universal reagent for genome tailoring. Genesis. 2000;26:99–109.

    Article  CAS  PubMed  Google Scholar 

  41. Kim H, Kim M, Im SK, Fang S. Mouse Cre-LoxP system: general principles to determine tissue-specific roles of target genes. Lab Anim Res. 2018;34:147–59.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Ramírez-Solis R, Liu P, Bradley A. Chromosome engineering in mice. Nature. 1995;378:720–4.

    Article  PubMed  Google Scholar 

  43. Baron U, Bujard H. Tet repressor-based system for regulated gene expression in eukaryotic cells: principles and advances. In: Methods in enzymology. Elsevier; 2000. p. 401–21.

    Google Scholar 

  44. Corti O, Sabaté O, Horellou P, Colin P, Dumas S, Buchet D, et al. A single adenovirus vector mediates doxycycline-controlled expression of tyrosine hydroxylase in brain grafts of human neural progenitors. Nat Biotechnol. 1999;17:349–54.

    Article  CAS  PubMed  Google Scholar 

  45. Corti O, Sánchez-Capelo A, Colin P, Hanoun N, Hamon M, Mallet J. Long-term doxycycline-controlled expression of human tyrosine hydroxylase after direct adenovirus-mediated gene transfer to a rat model of Parkinson’s disease. Proc Natl Acad Sci. 1999;96:12120–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Mansuy IM, Bujard H. Tetracycline-regulated gene expression in the brain. Curr Opin Neurobiol. 2000;10:593–6.

    Article  CAS  PubMed  Google Scholar 

  47. Smith AJH, De Sousa MA, Kwabi-Addo B, Heppell-Parton A, Impey H, Rabbitts P. A site–directed chromosomal translocation induced in embryonic stem cells by Cre-loxP recombination. Nat Genet. 1995;9:376–85.

    Article  CAS  PubMed  Google Scholar 

  48. Orban PC, Chui D, Marth JD. Tissue- and site-specific DNA recombination in transgenic mice. Proc Natl Acad Sci. 1992;89:6861–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Chen ZY, Jing D, Bath KG, Ieraci A, Khan T, Siao CJ, et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science. 2006;314:140–3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Robinson TE, Becker JB. Enduring changes in brain and behavior produced by chronic amphetamine administration: a review and evaluation of animal models of amphetamine psychosis. Brain Res Rev. 1986;11:157–98.

    Article  CAS  Google Scholar 

  51. Tenn CC, Kapur S, Fletcher PJ. Sensitization to amphetamine, but not phencyclidine, disrupts prepulse inhibition and latent inhibition. Psychopharmacology. 2005;180:366–76.

    Article  CAS  PubMed  Google Scholar 

  52. Deumens R, Blokland A, Prickaerts J. Modeling Parkinson’s disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp Neurol. 2002;175:303–17.

    Article  CAS  PubMed  Google Scholar 

  53. Czéh B, Fuchs E, Wiborg O, Simon M. Animal models of major depression and their clinical implications. Prog Neuro-Psychopharmacol Biol Psychiatry. 2016;64:293–310.

    Article  Google Scholar 

  54. Deisseroth K. Circuit dynamics of adaptive and maladaptive behaviour. Nature. 2014;505:309–17.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Steinberg EE, Christoffel DJ, Deisseroth K, Malenka RC. Illuminating circuitry relevant to psychiatric disorders with optogenetics. Curr Opin Neurobiol. 2015;30:9–16.

    Article  CAS  PubMed  Google Scholar 

  56. Porsolt RD, Le Pichon M, Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature. 1977;266(5604):730–2.

    Article  CAS  PubMed  Google Scholar 

  57. Steru L, Chermat R, Thierry B, Simon P. The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology. 1985;85:367–70.

    Article  CAS  PubMed  Google Scholar 

  58. Hiraoka K, Motomura K, Yanagida S, Ohashi A, Ishisaka-Furuno N, Kanba S. Pattern of c-Fos expression induced by tail suspension test in the mouse brain. Heliyon. 2017;3:e00316.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Can A, Dao DT, Terrillion CE, Piantadosi SC, Bhat S, Gould TD. The tail suspension test. J Vis Exp. 2012;(59):e3769.

    Google Scholar 

  60. Rosenberg MB, Carroll FI, Negus SS. Effects of monoamine reuptake inhibitors in assays of acute pain-stimulated and pain-depressed behavior in rats. J Pain. 2013;14:246–59.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Rafało-Ulińska A, Pałucha-Poniewiera A. The effectiveness of (R)-ketamine and its mechanism of action differ from those of (S)-ketamine in a chronic unpredictable mild stress model of depression in C57BL/6J mice. Behav Brain Res. 2022;418:113633.

    Article  PubMed  Google Scholar 

  62. Koprdová R, Bögi E, Belovičová K, Sedláčková N, Okuliarová M, Ujházy E, et al. Chronic unpredictable mild stress paradigm in male Wistar rats: effect on anxiety- and depressive-like behavior. Neuro Endocrinol Lett. 2016;37:103–10.

    PubMed  Google Scholar 

  63. Kudryavtseva NN, Bakshtanovskaya IV, Koryakina LA. Social model of depression in mice of C57BL/6J strain. Pharmacol Biochem Behav. 1991;38:315–20.

    Article  CAS  PubMed  Google Scholar 

  64. Kumar S, Hultman R, Hughes D, Michel N, Katz BM, Dzirasa K. Prefrontal cortex reactivity underlies trait vulnerability to chronic social defeat stress. Nat Commun. 2014;5:1–9.

    Article  CAS  Google Scholar 

  65. Planchez B, Surget A, Belzung C. Animal models of major depression: drawbacks and challenges. J Neural Transm. 2019;126:1383–408.

    Article  CAS  PubMed  Google Scholar 

  66. Becker C, Zeau B, Rivat C, Blugeot A, Hamon M, Benoliel JJ. Repeated social defeat-induced depression-like behavioral and biological alterations in rats: involvement of cholecystokinin. Mol Psychiatry. 2008;13:1079–92.

    Article  CAS  PubMed  Google Scholar 

  67. Mineur YS, Belzung C, Crusio WE. Effects of unpredictable chronic mild stress on anxiety and depression-like behavior in mice. Behav Brain Res. 2006;175:43–50.

    Article  PubMed  Google Scholar 

  68. Rygula R, Abumaria N, Flügge G, Fuchs E, Rüther E, Havemann-Reinecke U. Anhedonia and motivational deficits in rats: impact of chronic social stress. Behav Brain Res. 2005;162:127–34.

    Article  PubMed  Google Scholar 

  69. Kurre Nielsen C, Arnt J, Sánchez C. Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav Brain Res. 2000;107:21–33.

    Article  Google Scholar 

  70. Barik J, Marti F, Morel C, Fernandez SP, Lanteri C, Godeheu G, et al. Chronic stress triggers social aversion via glucocorticoid receptor in dopaminoceptive neurons. Science. 2013;339(6117):332–5.

    Article  CAS  PubMed  Google Scholar 

  71. Meerlo P, Overkamp GJF, Daan S, van den Hoofdakker RH, Koolhaas JM. Changes in behaviour and body weight following a single or double social defeat in rats. Stress. 1996;1:21–32.

    Article  CAS  PubMed  Google Scholar 

  72. Moreau JL, Jenck F, Martin JR, Mortas P, Haefely WE. Antidepressant treatment prevents chronic unpredictable mild stress-induced anhedonia as assessed by ventral tegmentum self-stimulation behavior in rats. Eur Neuropsychopharmacol. 1992;2:43–9.

    Article  CAS  PubMed  Google Scholar 

  73. Il P, J, Zhao T, Huang GB, Sui ZY, Li CR, Han EH, et al. Effects of aripiprazole and haloperidol on Fos-like immunoreactivity in the prefrontal cortex and amygdala. Clin Psychopharmacol Neurosci. 2011;9:36–43.

    Google Scholar 

  74. Serra M, Pisu MG, Floris I, Biggio G. Social isolation-induced changes in the hypothalamic–pituitary–adrenal axis in the rat. Stress. 2005;8:259–64.

    Article  CAS  PubMed  Google Scholar 

  75. Tye KM, Mirzabekov JJ, Warden MR, Ferenczi EA, Tsai HC, Finkelstein J, et al. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature. 2013;493:537–41.

    Article  CAS  PubMed  Google Scholar 

  76. Sarkar A, Kabbaj M. Sex differences in effects of ketamine on behavior, spine density, and synaptic proteins in socially isolated rats. Biol Psychiatry. 2016;80:448–56.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Markou A, Koob GF. Construct validity of a self-stimulation threshold paradigm: effects of reward and performance manipulations. Physiol Behav. 1992;51:111–9.

    Article  CAS  PubMed  Google Scholar 

  78. Rygula R, Abumaria N, Flügge G, Hiemke C, Fuchs E, Rüther E, et al. Citalopram counteracts depressive-like symptoms evoked by chronic social stress in rats. Behav Pharmacol. 2006;17:19–29.

    Article  CAS  PubMed  Google Scholar 

  79. Cordner ZA, Marshall-Thomas I, Boersma GJ, Lee RS, Potash JB, Tamashiro KLK. Fluoxetine and environmental enrichment similarly reverse chronic social stress-related depression- and anxiety-like behavior, but have differential effects on amygdala gene expression. Neurobiol Stress. 2021;15:100392.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Dournes C, Beeské S, Belzung C, Griebel G. Deep brain stimulation in treatment-resistant depression in mice: comparison with the CRF1 antagonist, SSR125543. Prog Neuro-Psychopharmacol Biol Psychiatry. 2013;40:213–20.

    Article  CAS  Google Scholar 

  81. Hamani C, Giacobbe P, Diwan M, Balbino ES, Tong J, Bridgman A, et al. Monoamine oxidase inhibitors potentiate the effects of deep brain stimulation. Am J Psychiatr. 2012;169:1320–1.

    Article  PubMed  Google Scholar 

  82. Hamani C, Machado DC, Hipólide DC, Dubiela FP, Suchecki D, Macedo CE, et al. Deep brain stimulation reverses anhedonic-like behavior in a chronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol Psychiatry. 2012;71:30–5.

    Article  CAS  PubMed  Google Scholar 

  83. Hamani C, Diwan M, Macedo CE, Brandão ML, Shumake J, Gonzalez-Lima F, et al. Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry. 2010;67:117–24.

    Article  PubMed  Google Scholar 

  84. Erburu M, Cajaleon L, Guruceaga E, Venzala E, Muñoz-Cobo I, Beltrán E, et al. Chronic mild stress and imipramine treatment elicit opposite changes in behavior and in gene expression in the mouse prefrontal cortex. Pharmacol Biochem Behav. 2015;135:227–36.

    Article  CAS  PubMed  Google Scholar 

  85. Zhang L, Luo J, Zhang M, Yao W, Ma X, Yu SY. Effects of curcumin on chronic, unpredictable, mild, stress-induced depressive-like behaviour and structural plasticity in the lateral amygdala of rats. Int J Neuropsychopharmacol. 2014;17:793–806.

    Article  CAS  PubMed  Google Scholar 

  86. Garzón J, Fuentes JA, Del Rio J. Antidepressants selectively antagonize the hyperactivity induced in rats by long-term isolation. Eur J Pharmacol. 1979;59:293–6.

    Article  PubMed  Google Scholar 

  87. Zazpe A, Artaiz I, Labeaga L, Lucero ML, Orjales A. Reversal of learned helplessness by selective serotonin reuptake inhibitors in rats is not dependent on 5-HT availability. Neuropharmacology. 2007;52:975–84.

    Article  CAS  PubMed  Google Scholar 

  88. Pereira VS, Joca SRL, Harvey BH, Elfving B, Wegener G. Esketamine and rapastinel, but not imipramine, have antidepressant-like effect in a treatment-resistant animal model of depression. Acta Neuropsychiatr. 2019;31:258–65.

    Article  PubMed  Google Scholar 

  89. Ciulla L, Menezes HS, Bueno BBM, Schuh A, Alves RJV, Abegg MP. Antidepressant behavioral effects of duloxetine and fluoxetine in the rat forced swimming test. Acta Cir Bras. 2007;22(5):351–4.

    Article  PubMed  Google Scholar 

  90. Rodríguez-Landa JF, Contreras CM, García-Ríos RI. Allopregnanolone microinjected into the lateral septum or dorsal hippocampus reduces immobility in the forced swim test: participation of the GABAA receptor. Behav Pharmacol. 2009;20:614–22.

    Article  PubMed  Google Scholar 

  91. Choi SH, Chung S, Cho JH, Cho YH, Im JWK, Kim JM, et al. Changes in c-Fos expression in the forced swimming test: common and distinct modulation in rat brain by desipramine and citalopram. Korean J Physiol Pharmacol. 2013;17:321–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Ma L, Xu Y, Wang G, Li R. What do we know about sex differences in depression: a review of animal models and potential mechanisms. Prog Neuro-Psychopharmacol Biol Psychiatry. 2019;89:48–56.

    Article  Google Scholar 

  93. Wang SM, Han C, Bahk WM, Lee SJ, Patkar AA, Masand PS, et al. Addressing the side effects of contemporary antidepressants: a comprehensive review. Chonnam Med J. 2018;54:101–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Gaynes BN, Lux L, Gartlehner G, Asher G, Forman-Hoffman V, Green J, et al. Defining treatment-resistant depression. Depress Anxiety. 2020;37:134–45.

    Article  PubMed  Google Scholar 

  95. Salahudeen MS, Wright CM, Peterson GM. Esketamine: new hope for the treatment of treatment-resistant depression? A narrative review. Ther Adv Drug Saf [Internet]. 2020 [cited 2022 July 23];11:2042098620937899. Available from: https://pubmed.ncbi.nlm.nih.gov/32782779/.

  96. Korte SM, Prins J, Krajnc AM, Hendriksen H, Oosting RS, Westphal KG, et al. The many different faces of major depression: it is time for personalized medicine. Eur J Pharmacol. 2015;753:88–104.

    Article  CAS  PubMed  Google Scholar 

  97. Walker DL, Toufexis DJ, Davis M. Role of the bed nucleus of the stria terminalis versus the amygdala in fear, stress, and anxiety. Eur J Pharmacol. 2003;463:199–216.

    Article  CAS  PubMed  Google Scholar 

  98. Lezak KR, Missig G, Carlezon WA Jr. Behavioral methods to study anxiety in rodents. Dialogues Clin Neurosci. 2017;19:181–91.

    Article  PubMed  PubMed Central  Google Scholar 

  99. Handley SL, Mithani S. Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear’-motivated behaviour. Naunyn Schmiedeberg's Arch Pharmacol. 1984;327:1–5.

    Article  CAS  Google Scholar 

  100. Crawley J, Goodwin FK. Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav. 1980;13:167–70.

    Article  CAS  PubMed  Google Scholar 

  101. Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology. 2009;204:361–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Himanshu D, Sarkar D, Nutan A. A review of behavioral tests to evaluate different types of anxiety and anti-anxiety effects. Clin Psychopharmacol Neurosci. 2020;18:341–51. Available from: https://pubmed.ncbi.nlm.nih.gov/32702213/.

    Article  CAS  PubMed Central  Google Scholar 

  103. Kleven MS, Koek W. Effects of benzodiazepine agonists on punished responding in pigeons and their relationship with clinical doses in humans. Psychopharmacology. 1999;141(2):206–12.

    Article  CAS  PubMed  Google Scholar 

  104. Oberrauch S, Sigrist H, Sautter E, Gerster S, Bach DR, Pryce CR. Establishing operant conflict tests for the translational study of anxiety in mice. Psychopharmacology. 2019;236:2527–41.

    Article  CAS  PubMed  Google Scholar 

  105. Ramirez K, Sheridan JF. Antidepressant imipramine diminishes stress-induced inflammation in the periphery and central nervous system and related anxiety-and depressive-like behaviors. Brain Behav Immun. 2016;57:293–303.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Moreira CM, Masson S, Carvalho MC, Brandão ML. Exploratory behaviour of rats in the elevated plus-maze is differentially sensitive to inactivation of the basolateral and central amygdaloid nuclei. Brain Res Bull. 2007;71:466–74.

    Article  PubMed  Google Scholar 

  107. Sanchez C, Meier E. Behavioral profiles of SSRIs in animal models of depression, anxiety and aggression. Are they all alike? Psychopharmacology. 1997;129:197–201.

    Article  CAS  PubMed  Google Scholar 

  108. Strawn JR, Geracioti L, Rajdev N, Clemenza K, Levine A. Pharmacotherapy for generalized anxiety disorder in adults and pediatric patients: an evidence-based treatment review. Expert Opin Pharmacother. 2018;19:1057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Sartori SB, Singewald N. Novel pharmacological targets in drug development for the treatment of anxiety and anxiety-related disorders. Pharmacol Ther. 2019;204:107402.

    Article  CAS  PubMed  Google Scholar 

  110. Colucci P, Marchetta E, Mancini GF, Alva P, Chiarotti F, Hasan MT, et al. Predicting susceptibility and resilience in an animal model of post-traumatic stress disorder (PTSD). Transl Psychiatry. 2020;10:243.

    Article  PubMed  PubMed Central  Google Scholar 

  111. Knox D, George SA, Fitzpatrick CJ, Rabinak CA, Maren S, Liberzon I. Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem. 2012;19:43–9.

    Article  PubMed  PubMed Central  Google Scholar 

  112. Jacobson-Pick S, Audet MC, McQuaid RJ, Kalvapalle R, Anisman H. Social agonistic distress in male and female mice: changes of behavior and brain monoamine functioning in relation to acute and chronic challenges. PLoS One. 2013;8:e60133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Zoladz PR, Conrad CD, Fleshner M, Diamond DM. Acute episodes of predator exposure in conjunction with chronic social instability as an animal model of post-traumatic stress disorder. Stress. 2008;11:259–81.

    Article  PubMed  PubMed Central  Google Scholar 

  114. Cohen H, Zohar J, Matar M. The relevance of differential response to trauma in an animal model of posttraumatic stress disorder. Biol Psychiatry. 2003;53:463–73.

    Article  PubMed  Google Scholar 

  115. Bentefour Y, Rakibi Y, Bennis M, Ba-M’hamed S, Garcia R. Paroxetine treatment, following behavioral suppression of PTSD-like symptoms in mice, prevents relapse by activating the infralimbic cortex. Eur Neuropsychopharmacol. 2016;26:195–207.

    Article  CAS  PubMed  Google Scholar 

  116. Reisman M. PTSD treatment for veterans: what’s working, what’s new, and what’s next. P T. 2016;41:623.

    PubMed  PubMed Central  Google Scholar 

  117. Richter-Levin G, Stork O, Schmidt MV. Animal models of PTSD: a challenge to be met. Mol Psychiatry. 2019;24:1135–56.

    Article  PubMed  Google Scholar 

  118. Becker A, Grecksch G, Bernstein HG, Höllt V, Bogerts B. Social behaviour in rats lesioned with ibotenic acid in the hippocampus: quantitative and qualitative analysis. Psychopharmacology. 1999;144:333–8.

    Article  CAS  PubMed  Google Scholar 

  119. Talamini LM, Ellenbroek B, Koch T, Korf J. Impaired sensory gating and attention in rats with developmental abnormalities of the mesocortex: implications for schizophrenia. Ann N Y Acad Sci. 2000;911:486–94.

    Article  CAS  PubMed  Google Scholar 

  120. Lodge DJ, Grace AA. Gestational methylazoxymethanol acetate administration: a developmental disruption model of schizophrenia. Behav Brain Res. 2009;204:306–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Moore H, Jentsch JD, Ghajarnia M, Geyer MA, Grace AA. A neurobehavioral systems analysis of adult rats exposed to methylazoxymethanol acetate on E17: implications for the neuropathology of schizophrenia. Biol Psychiatry. 2006;60:253–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Jentsch JD, Taylor JR, Roth RH. Subchronic phencyclidine administration increases mesolimbic dopaminergic system responsivity and augments stress- and psychostimulant-induced hyperlocomotion. Neuropsychopharmacology. 1998;19:105–13.

    Article  CAS  PubMed  Google Scholar 

  123. Kocsis B, Brown RE, McCarley RW, Hajos M. Impact of ketamine on neuronal network dynamics: translational modeling of schizophrenia-relevant deficits. CNS Neurosci Ther. 2013;19:437–47.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Featherstone RE, Rizos Z, Kapur S, Fletcher PJ. A sensitizing regimen of amphetamine that disrupts attentional set-shifting does not disrupt working or long-term memory. Behav Brain Res. 2008;189:170–9.

    Article  CAS  PubMed  Google Scholar 

  125. Pletnikov MV, Ayhan Y, Nikolskaia O, Xu Y, Ovanesov MV, Huang H, et al. Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia. Mol Psychiatry. 2008;13:173–86.

    Article  CAS  PubMed  Google Scholar 

  126. Bassett AS, Chow EWC, Husted J, Weksberg R, Caluseriu O, Webb GD, et al. Clinical features of 78 adults with 22q11 deletion syndrome. Am J Med Genet A. 2005;138A:307–13.

    Article  Google Scholar 

  127. Saito R, Miyoshi C, Koebis M, Kushima I, Nakao K, Mori D, et al. Two novel mouse models mimicking minor deletions in 22q11.2 deletion syndrome revealed the contribution of each deleted region to psychiatric disorders. Mol Brain. 2021;14:68.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Nakazawa T, Kikuchi M, Ishikawa M, Yamamori H, Nagayasu K, Matsumoto T, et al. Differential gene expression profiles in neurons generated from lymphoblastoid B-cell line-derived iPS cells from monozygotic twin cases with treatment-resistant schizophrenia and discordant responses to clozapine. Schizophr Res. 2017;181:75–82.

    Article  PubMed  Google Scholar 

  129. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature. 2011;473:221–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Amann LC, Gandal MJ, Halene TB, Ehrlichman RS, White SL, McCarren HS, et al. Mouse behavioral endophenotypes for schizophrenia. Brain Res Bull. 2010;83:147–61.

    Article  PubMed  Google Scholar 

  131. van den Buuse M, Gogos A. Differential effects of antipsychotic drugs on serotonin-1A receptor-mediated disruption of prepulse inhibition. J Pharmacol Exp Ther. 2007;320:1224.

    Article  PubMed  Google Scholar 

  132. Sampaio LRL, Cysne Filho FMS, de Almeida JC, dos Santos Diniz D, de Sousa CNS, Sampaio LRL, et al. Advantages of the alpha-lipoic acid association with chlorpromazine in a model of schizophrenia induced by ketamine in rats: behavioral and oxidative stress evidences. Neuroscience. 2018;373:72–81.

    Article  CAS  PubMed  Google Scholar 

  133. Tandon R, Lenderking WR, Weiss C, Shalhoub H, Barbosa CD, Chen J, et al. The impact on functioning of second-generation antipsychotic medication side effects for patients with schizophrenia: a worldwide, cross-sectional, web-based survey. Ann General Psychiatry. 2020;19:1–11.

    Google Scholar 

  134. Potkin SG, Kane JM, Correll CU, Lindenmayer JP, Agid O, Marder SR, et al. The neurobiology of treatment-resistant schizophrenia: paths to antipsychotic resistance and a roadmap for future research. NPJ Schizophr. 2020;6:1–10.

    Article  PubMed  PubMed Central  Google Scholar 

  135. Robinson TE, Berridge KC. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Rev. 1993;18:247–91.

    Article  CAS  PubMed  Google Scholar 

  136. Steketee JD, Kalivas PW. Drug wanting: behavioral sensitization and relapse to drug-seeking behavior. Sibley DR, editor. Pharmacol Rev. 2011;63:348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Janetsian SS, Linsenbardt DN, Lapish CC. Memory impairment and alterations in prefrontal cortex gamma band activity following methamphetamine sensitization. Psychopharmacology. 2015;232:2083–95.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Mucha RF, van der Kooy D, O’Shaughnessy M, Bucenieks P. Drug reinforcement studied by the use of place conditioning in rat. Brain Res. 1982;243:91–105.

    Article  CAS  PubMed  Google Scholar 

  139. Ahmed SH, Koob GF. Transition from moderate to excessive drug intake: change in hedonic set point. Science. 1979;1998(282):298–300.

    Google Scholar 

  140. Mandt BH, Copenhagen LI, Zahniser NR, Allen RM. Escalation of cocaine consumption in short and long access self-administration procedures. Drug Alcohol Depend. 2015;149:166–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Wang Z-Y, Guo L-K, Han X, Song R, Dong G-M, Ma C-M, et al. Naltrexone attenuates methamphetamine-induced behavioral sensitization and conditioned place preference in mice. Behav Brain Res. 2021;399:112971.

    Article  CAS  PubMed  Google Scholar 

  142. Kaplan LM, Vella L, Cabral E, Tieu L, Ponath C, Guzman D, et al. Unmet mental health and substance use treatment needs among older homeless adults: results from the HOPE HOME study. J Community Psychol. 2019;47:1893–908.

    Article  PubMed  PubMed Central  Google Scholar 

  143. Gainetdinov RR, Caron MG. An animal model of attention deficit hyperactivity disorder. Mol Med Today. 2000;6:43–4.

    Article  CAS  PubMed  Google Scholar 

  144. Trinh JV, Nehrenberg DL, Jacobsen JPR, Caron MG, Wetsel WC. Differential psychostimulant-induced activation of neural circuits in dopamine transporter knockout and wild type mice. Neuroscience. 2003;118:297–310.

    Article  CAS  PubMed  Google Scholar 

  145. Zhou M, Rebholz H, Brocia C, Warner-Schmidt JL, Fienberg AA, Nairn AC, et al. Forebrain overexpression of CK1delta leads to down-regulation of dopamine receptors and altered locomotor activity reminiscent of ADHD. Proc Natl Acad Sci U S A. 2010;107:4401–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Yan TC, Hunt SP, Stanford SC. Behavioural and neurochemical abnormalities in mice lacking functional tachykinin-1 (NK1) receptors: a model of attention deficit hyperactivity disorder. Neuropharmacology. 2009;57:627–35.

    Article  CAS  PubMed  Google Scholar 

  147. Yan TC, Dudley JA, Weir RK, Grabowska EM, Peña-Oliver Y, Ripley TL, et al. Performance deficits of NK1 receptor knockout mice in the 5-choice serial reaction-time task: effects of d-amphetamine, stress and time of day. PLoS One. 2011;6:e17586–6.

    Google Scholar 

  148. Simchon Y, Weizman A, Rehavi M. The effect of chronic methylphenidate administration on presynaptic dopaminergic parameters in a rat model for ADHD. Eur Neuropsychopharmacol. 2010;20:714–20.

    Article  CAS  PubMed  Google Scholar 

  149. Sagvolden T. Behavioral validation of the spontaneously hypertensive rat (SHR) as an animal model of attention-deficit/hyperactivity disorder (AD/HD). Neurosci Biobehav Rev. 2000;24:31–9.

    Article  CAS  PubMed  Google Scholar 

  150. Bayless DW, Perez MC, Daniel JM. Comparison of the validity of the use of the spontaneously hypertensive rat as a model of attention deficit hyperactivity disorder in males and females. Behav Brain Res. 2015;286:85–92.

    Article  PubMed  Google Scholar 

  151. Evenden JL. Varieties of impulsivity. Psychopharmacology. 1999;146:348–61.

    Article  CAS  PubMed  Google Scholar 

  152. Robbins T. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology. 2002;163:362–80.

    Article  CAS  PubMed  Google Scholar 

  153. Navarra R, Graf R, Huang Y, Logue S, Comery T, Hughes Z, et al. Effects of atomoxetine and methylphenidate on attention and impulsivity in the 5-choice serial reaction time test. Prog Neuro-Psychopharmacol Biol Psychiatry. 2008;32:34–41.

    Article  CAS  Google Scholar 

  154. Umehara M, Ago Y, Kawanai T, Fujita K, Hiramatsu N, Takuma K, et al. Methylphenidate and venlafaxine attenuate locomotion in spontaneously hypertensive rats, an animal model of attention–deficit/hyperactivity disorder, through α2-adrenoceptor activation. Behav Pharmacol. 2013;24:328–31.

    Article  CAS  PubMed  Google Scholar 

  155. Sagvolden T. Impulsiveness, overactivity, and poorer sustained attention improve by chronic treatment with low doses of l-amphetamine in an animal model of attention-deficit/hyperactivity disorder (ADHD). Behav Brain Funct. 2011;7:1–10.

    Article  Google Scholar 

  156. Caye A, Swanson JM, Coghill D, Rohde LA. Treatment strategies for ADHD: an evidence-based guide to select optimal treatment. Mol Psychiatry. 2018;24(3):390–408.

    Article  PubMed  Google Scholar 

  157. Prossnitz ER, Arterburn JB. International union of basic and clinical pharmacology. XCVII. G protein-coupled estrogen receptor and its pharmacologic modulators. Pharmacol Rev. 2015;67:505–40.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Montague D, Weickert CS, Tomaskovic-Crook E, Rothmond DA, Kleinman JE, Rubinow DR. Oestrogen receptor alpha localisation in the prefrontal cortex of three mammalian species. J Neuroendocrinol. 2008;20(7):893–903.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Kritzer MF. Regional, laminar, and cellular distribution of immunoreactivity for ERα and ERβ in the cerebral cortex of hormonally intact, adult male and female rats. Cereb Cortex. 2002;12:116–28.

    Article  CAS  PubMed  Google Scholar 

  160. Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-α and -β mRNA in the rat central nervous system. J Comp Neurol. 1997;388:507–25.

    Article  CAS  PubMed  Google Scholar 

  161. González M, Cabrera-Socorro A, Pérez-García CG, Fraser JD, López FJ, Alonso R, et al. Distribution patterns of estrogen receptor α and β in the human cortex and hippocampus during development and adulthood. J Comp Neurol. 2007;503:790–802.

    Article  PubMed  Google Scholar 

  162. Ostlund H, Keller E, Hurd YL. Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann N Y Acad Sci. 2003;1007:54–63.

    Article  PubMed  Google Scholar 

  163. Simerly RB, Swanson LW, Chang C, Muramatsu M. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol. 1990;294:76–95.

    Article  CAS  PubMed  Google Scholar 

  164. Gasiorowska A, Wydrych M, Drapich P, Zadrozny M, Steczkowska M, Niewiadomski W, et al. The biology and pathobiology of glutamatergic, cholinergic, and dopaminergic signaling in the aging brain. Front Aging Neurosci. 2021;13:654931.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Forester BP, Parikh SV, Weisenbach S, Ajilore O, Vahia I, Rothschild AJ, et al. Combinatorial pharmacogenomic testing improves outcomes for older adults with depression. Am J Geriatr Psychiatry. 2020;28:933–45.

    Article  PubMed  Google Scholar 

  166. Henke H, Lang W. Cholinergic enzymes in neocortex, hippocampus and basal forebrain of non-neurological and senile dementia of Alzheimer-type patients. Brain Res. 1983;267:281–91.

    Article  CAS  PubMed  Google Scholar 

  167. Kumar A, Foster TC. Alteration in NMDA receptor mediated glutamatergic neurotransmission in the hippocampus during senescence. Neurochem Res. 2019;44:38–48.

    Article  CAS  PubMed  Google Scholar 

  168. Luo Z, Ahlers-Dannen KE, Spicer MM, Yang J, Alberico S, Stevens HE, et al. Age-dependent nigral dopaminergic neurodegeneration and α-synuclein accumulation in RGS6-deficient mice. JCI Insight. 2019;5(13):e126769.

    Article  PubMed  Google Scholar 

  169. Backstrom T, Sanders D, Leask R, Davidson D, Warner P, Bancroft J. Mood, sexuality, hormones, and the menstrual cycle. II. Hormone levels and their relationship to the premenstrual syndrome. Psychosom Med. 1983;45(6):503–7.

    Article  CAS  PubMed  Google Scholar 

  170. Benazzi F. Prevalence and clinical features of atypical depression in depressed outpatients: a 467-case study. Psychiatry Res. 1999;86:259–65.

    Article  CAS  PubMed  Google Scholar 

  171. Marcus SM, Young EA, Kerber KB, Kornstein S, Farabaugh AH, Mitchell J, et al. Gender differences in depression: findings from the STAR*D study. J Affect Disord. 2005;87:141–50.

    Article  PubMed  Google Scholar 

  172. Marcus SM, Kerber KB, Rush AJ, Wisniewski SR, Nierenberg A, Balasubramani GK, et al. Sex differences in depression symptoms in treatment-seeking adults: confirmatory analyses from the sequenced treatment alternatives to relieve depression study. Compr Psychiatry. 2008;49:238–46.

    Article  PubMed  PubMed Central  Google Scholar 

  173. Kornstein SG, Young EA, Harvey AT, Wisniewski SR, Barkin JL, Thase ME, et al. The influence of menopause status and postmenopausal use of hormone therapy on presentation of major depression in women. Menopause. 2010;17(4):828–39.

    Article  PubMed  PubMed Central  Google Scholar 

  174. Koss WA, Einat H, Schloesser RJ, Manji HK, Rubinow DR. Estrogen effects on the forced swim test differ in two outbred rat strains. Physiol Behav. 2012;106:81–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Marvan ML, Chavez-Chavez L, Santana S. Clomipramine modifies fluctuations of forced swimming immobility in different phases of the rat estrous cycle. Arch Med Res. 1996;27:83–6.

    CAS  PubMed  Google Scholar 

  176. Padilla E, Barrett D, Shumake J, Gonzalez-Lima F. Strain, sex, and open-field behavior: factors underlying the genetic susceptibility to helplessness. Behav Brain Res. 2009;201:257–64.

    Article  PubMed  PubMed Central  Google Scholar 

  177. Shors TJ, Mathew J, Sisti HM, Edgecomb C, Beckoff S, Dalla C. Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol Psychiatry. 2007;62:487–95.

    Article  PubMed  PubMed Central  Google Scholar 

  178. Konkle ATM, Baker SL, Kentner AC, Barbagallo LSM, Merali Z, Bielajew C. Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared. Brain Res. 2003;992:227–38.

    Article  CAS  PubMed  Google Scholar 

  179. Jablensky A, McGrath J, Herrman H, Castle D, Gureje O, Evans M, et al. Psychotic disorders in urban areas: an overview of the study on low prevalence disorders. Aust N Z J Psychiatry. 2000;34:221–36.

    Article  CAS  PubMed  Google Scholar 

  180. Breslau N, Chilcoat HD, Kessler RC, Peterson EL, Lucia VC. Vulnerability to assaultive violence: further specification of the sex difference in post-traumatic stress disorder. Psychol Med. 1999;29:813–21.

    Article  CAS  PubMed  Google Scholar 

  181. Olff M, Langeland W, Draijer N, Gersons BPR. Gender differences in posttraumatic stress disorder. Psychol Bull. 2007;133:183–204.

    Article  PubMed  Google Scholar 

  182. De Jongh R, Geyer MA, Olivier B, Groenink L. The effects of sex and neonatal maternal separation on fear-potentiated and light-enhanced startle. Behav Brain Res. 2005;161:190–6.

    Article  PubMed  Google Scholar 

  183. Maren S, De Oca B, Fanselow MS. Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res. 1994;661:25–34.

    Article  CAS  PubMed  Google Scholar 

  184. Kornstein SG, Schatzberg AF, Thase ME, Yonkers KA, McCullough JP, Keitner GI, et al. Gender differences in treatment response to sertraline versus imipramine in chronic depression. Am J Psychiatr. 2000;157:1445–52.

    Article  CAS  PubMed  Google Scholar 

  185. Henkel V, Mergl R, Allgaier AK, Kohnen R, Möller HJ, Hegerl U. Treatment of depression with atypical features: a meta-analytic approach. Psychiatry Res. 2006;141:89–101.

    Article  PubMed  Google Scholar 

  186. Usall J, Suarez D, Haro JM. Gender differences in response to antipsychotic treatment in outpatients with schizophrenia. Psychiatry Res. 2007;153:225–31.

    Article  CAS  PubMed  Google Scholar 

  187. Schmidt R, Baumann F, Hanschmann H, Geissler F, Preiss R. Gender difference in ifosfamide metabolism by human liver microsomes. Eur J Drug Metab Pharmacokinet. 2001;26:193–200.

    Article  CAS  PubMed  Google Scholar 

  188. Cuzzolin L, Schinella M, Tellini U, Pezzoli L, Lippi U, Benoni G. The effect of sex and cardiac failure on the pharmacokinetics of a slow-release theophylline formulation in the elderly. Pharmacol Res. 1990;22:137–8.

    Article  PubMed  Google Scholar 

  189. Prior TI, Baker GB. Interactions between the cytochrome P450 system and the second-generation antipsychotics. J Psychiatry Neurosci. 2003;28:99–112.

    PubMed  PubMed Central  Google Scholar 

  190. Timmer CJ, Sitsen JM, Delbressine LP. Clinical pharmacokinetics of mirtazapine. Clin Pharmacokinet. 2000;38:461–74.

    Article  CAS  PubMed  Google Scholar 

  191. Abernethy DR, Greenblatt DJ, Shader RI. Imipramine and desipramine disposition in the elderly. J Pharmacol Exp Ther. 1985;232:183–8.

    CAS  PubMed  Google Scholar 

  192. Ilic K, Hawke RL, Thirumaran RK, Schuetz EG, Hull JH, Kashuba ADM, et al. Influences on CYP2B6 activity using bupropion. Drug Metab Dispos. 2013;41:575.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  193. Benet LZ, Izumi T, Zhang Y, Silverman JA, Wacher VJ. Intestinal MDR transport proteins and P-450 enzymes as barriers to oral drug delivery. J Control Release. 1999;62:25–31.

    Article  CAS  PubMed  Google Scholar 

  194. O’Brien FE, O’Connor RM, Clarke G, Dinan TG, Griffin BT, Cryan JF. P-glycoprotein inhibition increases the brain distribution and antidepressant-like activity of escitalopram in rodents. Neuropsychopharmacology. 2013;38(11):2209–19.

    Article  PubMed  PubMed Central  Google Scholar 

  195. Bradford LD. CYP2D6 allele frequency in European Caucasians, Asians, Africans and their descendants. Pharmacogenomics. 2002;3:229–43.

    Article  CAS  PubMed  Google Scholar 

  196. Hwang WJ, Lee TY, Kim NS, Kwon JS. The role of estrogen receptors and their Signaling across psychiatric disorders. Int J Mol Sci. 2020;22:373.

    Article  PubMed  PubMed Central  Google Scholar 

  197. Kokras N, Dalla C. Sex differences in animal models of psychiatric disorders. Br J Pharmacol. 2014;171:4595–619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  198. Weiner DM, Levey AI, Brann MR. Expression of muscarinic acetylcholine and dopamine receptor mRNAs in rat basal ganglia. Proc Natl Acad Sci. 1990;87:7050–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  199. Vilaró MT, Palacios JM, Mengod G. Localization of m5 muscarinic receptor mRNA in rat brain examined by in situ hybridization histochemistry. Neurosci Lett. 1990;114:154–9.

    Article  PubMed  Google Scholar 

  200. Yamada M, Lamping KG, Duttaroy A, Zhang W, Cui Y, Bymaster FP, et al. Cholinergic dilation of cerebral blood vessels is abolished in M5 muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci. 2001;98:14096–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Basile AS, Fedorova I, Zapata A, Liu X, Shippenberg T, Duttaroy A, et al. Deletion of the M5 muscarinic acetylcholine receptor attenuates morphine reinforcement and withdrawal but not morphine analgesia. Proc Natl Acad Sci. 2002;99:11452–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  202. Fink-Jensen A, Fedorova I, Wörtwein G, Woldbye DPD, Rasmussen T, Thomsen M, et al. Role for M5 muscarinic acetylcholine receptors in cocaine addiction. J Neurosci Res. 2003;74:91–6.

    Article  CAS  PubMed  Google Scholar 

  203. Steidl S, Yeomans JS. M5 muscarinic receptor knockout mice show reduced morphine-induced locomotion but increased locomotion after cholinergic antagonism in the ventral tegmental area. J Pharmacol Exp Ther. 2009;328:263–75.

    Article  CAS  PubMed  Google Scholar 

  204. Katz RJ. Animal model of depression: pharmacological sensitivity of a hedonic deficit. Pharmacol Biochem Behav. 1982;16:965–8.

    Article  CAS  PubMed  Google Scholar 

  205. Kessler RC. The effects of stressful life events on depression. Annu Rev Psychol. 1997;48:191–214.

    Article  CAS  PubMed  Google Scholar 

  206. Javitt DC, Carter CS, Krystal JH, Kantrowitz JT, Girgis RR, Kegeles LS, et al. Utility of imaging-based biomarkers for glutamate-targeted drug development in psychotic disorders: a randomized clinical trial. JAMA Psychiat. 2018;75:11–9.

    Article  Google Scholar 

  207. De Simoni S, Schwarz AJ, O’Daly OG, Marquand AF, Brittain C, Gonzales C, et al. Test–retest reliability of the BOLD pharmacological MRI response to ketamine in healthy volunteers. NeuroImage. 2013;64:75–90.

    Article  PubMed  Google Scholar 

  208. Kantrowitz JT, Grinband J, Goff DC, Lahti AC, Marder SR, Kegeles LS, et al. Proof of mechanism and target engagement of glutamatergic drugs for the treatment of schizophrenia: RCTs of pomaglumetad and TS-134 on ketamine-induced psychotic symptoms and pharmacoBOLD in healthy volunteers. Neuropsychopharmacology. 2020;45(11):1842–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  209. Littlewood CL, Jones N, O’Neill MJ, Mitchell SN, Tricklebank M, Williams SCR. Mapping the central effects of ketamine in the rat using pharmacological MRI. Psychopharmacology. 2006;186:64–81.

    Article  CAS  PubMed  Google Scholar 

  210. Chin CL, Upadhyay J, Marek GJ, Baker SJ, Zhang M, Mezler M, et al. Awake rat pharmacological magnetic resonance imaging as a translational pharmacodynamic biomarker: metabotropic glutamate 2/3 agonist modulation of ketamine-induced blood oxygenation level dependence signals. J Pharmacol Exp Ther. 2011;336:709–15.

    Article  CAS  PubMed  Google Scholar 

  211. Wadenberg MLG, Kapur S, Soliman A, Jones C, Vaccarino F. Dopamine D2 receptor occupancy predicts catalepsy and the suppression of conditioned avoidance response behaviour in rats. Psychopharmacology. 2000;150:422–9.

    Article  CAS  PubMed  Google Scholar 

  212. Wadenberg MLG. Conditioned avoidance response in the development of new antipsychotics. Curr Pharm Des. 2010;16:358–70.

    Article  CAS  PubMed  Google Scholar 

  213. Kapur S, Zipursky R, Jones C, Remington G, Houle S. Relationship between dopamine D2 occupancy, clinical response, and side effects: a double-blind PET study of first-episode schizophrenia. Am J Psychiatr. 2000;157:514–20.

    Article  CAS  PubMed  Google Scholar 

  214. Farde L, Nordström AL, Wiesel FA, Pauli S, Halldin C, Sedvall G. Positron emission tomographic analysis of central D1 and D2 dopamine receptor occupancy in patients treated with classical neuroleptics and clozapine: relation to extrapyramidal side effects. Arch Gen Psychiatry. 1992;49:538–44.

    Article  CAS  PubMed  Google Scholar 

  215. Pfurtscheller G, Lopes da Silva FH. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clin Neurophysiol. 1999;110:1842–57.

    Article  CAS  PubMed  Google Scholar 

  216. Medithe JWC, Nelakuditi UR. Study of normal and abnormal EEG. In: 2016 3rd international conference on advanced computing and communication systems (ICACCS). IEEE; 2016. p. 1–4.

    Google Scholar 

  217. Sullivan D, Mizuseki K, Sorgi A, Buzsáki G. Comparison of sleep spindles and theta oscillations in the hippocampus. J Neurosci. 2014;34:662.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  218. Morairty SR, Hedley L, Flores J, Martin R, Kilduff TS. Selective 5HT2A and 5HT6 receptor antagonists promote sleep in rats. Sleep. 2008;31:34–44.

    Article  PubMed  PubMed Central  Google Scholar 

  219. Bubser M, Byun NE, Wood MR, Jones CK. Muscarinic receptor pharmacology and circuitry for the modulation of cognition. Handb Exp Pharmacol. 2011;208:121–66.

    Article  Google Scholar 

  220. Shekhar A, Potter WZ, Lightfoot J, Lienemann J, Dubé S, Mallinckrodt C, et al. Selective muscarinic receptor agonist xanomeline as a novel treatment approach for schizophrenia. Am J Psychiatr. 2008;165:1033–9.

    Article  PubMed  Google Scholar 

  221. Gomeza J, Zhang L, Kostenis E, Felder C, Bymaster F, Brodkin J, et al. Enhancement of D1 dopamine receptor-mediated locomotor stimulation in M(4) muscarinic acetylcholine receptor knockout mice. Proc Natl Acad Sci U S A. 1999;96:10483–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Brady AE, Jones CK, Bridges TM, Kennedy JP, Thompson AD, Heiman JU, et al. Centrally active allosteric potentiators of the M4 muscarinic acetylcholine receptor reverse amphetamine-induced hyperlocomotor activity in rats. J Pharmacol Exp Ther. 2008;327:941–53.

    Article  CAS  PubMed  Google Scholar 

  223. Byun NE, Grannan M, Bubser M, Barry RL, Thompson A, Rosanelli J, et al. Antipsychotic drug-like effects of the selective M4 muscarinic acetylcholine receptor positive allosteric modulator VU0152100. Neuropsychopharmacology. 2014;39:1578–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Shigemoto R, Mizuno N. Chapter III Metabotropic glutamate receptors — immunocytochemical and in situ hybridization analyses. In: Handbook of chemical neuroanatomy, vol. 18. Elsevier; 2000. p. 63–98.

    Google Scholar 

  225. Luján R, Roberts JDB, Shigemoto R, Ohishi H, Somogyi P. Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1α, mGluR2 and mGluR5, relative to neurotransmitter release sites. J Chem Neuroanat. 1997;13:219–41.

    Article  PubMed  Google Scholar 

  226. Kuwajima M, Hall RA, Aiba A, Smith Y. Subcellular and subsynaptic localization of group I metabotropic glutamate receptors in the monkey subthalamic nucleus. J Comp Neurol. 2004;474:589–602.

    Article  CAS  PubMed  Google Scholar 

  227. Gasparini F, Lingenhöhl K, Stoehr N, Flor PJ, Heinrich M, Vranesic I, et al. 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology. 1999;38:1493–503.

    Article  CAS  PubMed  Google Scholar 

  228. Cosford NDP, Tehrani L, Roppe J, Schweiger E, Smith ND, Anderson J, et al. 3-[(2-Methyl-1,3-thiazol-4-yl)ethynyl]-pyridine: a potent and highly selective metabotropic glutamate subtype 5 receptor antagonist with anxiolytic activity. J Med Chem. 2003;46:204–6.

    Article  CAS  PubMed  Google Scholar 

  229. Liu CY, Jiang XX, Zhu YH, Wei DN. Metabotropic glutamate receptor 5 antagonist 2-methyl-6-(phenylethynyl)pyridine produces antidepressant effects in rats: role of brain-derived neurotrophic factor. Neuroscience. 2012;223:219–24.

    Article  CAS  PubMed  Google Scholar 

  230. Li X, Need AB, Baez M, Witkin JM. Metabotropic glutamate 5 receptor antagonism is associated with antidepressant-like effects in mice. J Pharmacol Exp Ther. 2006;319:254–9.

    Article  CAS  PubMed  Google Scholar 

  231. Lindemann L, Jaeschke G, Michalon A, Vieira E, Honer M, Spooren W, et al. CTEP: a novel, potent, long-acting, and orally bioavailable metabotropic glutamate receptor 5 inhibitor. J Pharmacol Exp Ther. 2011;339:474–86.

    Article  CAS  PubMed  Google Scholar 

  232. Lindemann L, Porter RH, Scharf SH, Kuennecke B, Bruns A, Von Kienlin M, et al. Pharmacology of basimglurant (RO4917523, RG7090), a unique metabotropic glutamate receptor 5 negative allosteric modulator in clinical development for depression. J Pharmacol Exp Ther. 2015;353:213–33.

    Article  CAS  PubMed  Google Scholar 

  233. Ametamey SM, Kessler LJ, Honer M, Wyss MT, Buck A, Hintermann S, et al. Radiosynthesis and preclinical evaluation of 11 C-ABP688 as a probe for imaging the metabotropic glutamate receptor subtype 5. J Nucl Med. 2006;47:698–705.

    CAS  PubMed  Google Scholar 

  234. Steiger A, Pawlowski M. Depression and sleep. Int J Mol Sci. 2019;20(3):607.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  235. Mayers AG, Baldwin DS. Antidepressants and their effect on sleep. Hum Psychopharmacol. 2005;20:533–59.

    Article  CAS  PubMed  Google Scholar 

  236. Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry. 1979;134:382–9.

    Article  CAS  PubMed  Google Scholar 

  237. Quiroz JA, Tamburri P, Deptula D, Banken L, Beyer U, Rabbia M, et al. Efficacy and safety of basimglurant as adjunctive therapy for major depression: a randomized clinical trial. JAMA Psychiat. 2016;73:675–84.

    Article  Google Scholar 

  238. Belzung C. Innovative drugs to treat depression: did animal models fail to be predictive or did clinical trials fail to detect effects. Neuropsychopharmacology. 2014;39:1041–51.

    Article  PubMed  PubMed Central  Google Scholar 

  239. McGonigle P, Ruggeri B. Animal models of human disease: challenges in enabling translation. Biochem Pharmacol. 2014;87:162–71.

    Article  CAS  PubMed  Google Scholar 

  240. Cuthbert BN, Insel TR. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med. 2013;11:126.

    Article  PubMed  PubMed Central  Google Scholar 

  241. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatr. 2010;167:748–51.

    Article  PubMed  Google Scholar 

  242. Cuthbert BN. Research domain criteria: toward future psychiatric nosologies. Dialogues Clin Neurosci. 2015;17:89–97.

    Article  PubMed  PubMed Central  Google Scholar 

  243. Hyman SE. Use of mouse models to investigate the contributions of CNVs associated with schizophrenia and autism to disease mechanisms. Curr Opin Genet Dev. 2021;68:99–105.

    Article  CAS  PubMed  Google Scholar 

  244. Mali P, Esvelt KM, Church GM. Cas9 as a versatile tool for engineering biology. Nat Methods. 2013;10:957–63.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  245. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 2012;337:816–21.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  246. Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L, Kempton HR, et al. CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell. 2014;159:440–55.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Zhao H, Tu Z, Xu H, Yan S, Yan H, Zheng Y, et al. Altered neurogenesis and disrupted expression of synaptic proteins in prefrontal cortex of SHANK3-deficient non-human primate. Cell Res. 2017;27:1293–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  248. Moessner R, Marshall CR, Sutcliffe JS, Skaug J, Pinto D, Vincent J, et al. Contribution of SHANK3 mutations to autism spectrum disorder. Am J Hum Genet. 2007;81:1289–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  249. Tu Z, Zhao H, Li B, Yan S, Wang L, Tang Y, et al. CRISPR/Cas9-mediated disruption of SHANK3 in monkey leads to drug-treatable autism-like symptoms. Hum Mol Genet. 2019;28:561–71.

    Article  CAS  PubMed  Google Scholar 

  250. Boyden ES, Zhang F, Bamberg E, Nagel G, Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci. 2005;8:1263–8.

    Article  CAS  PubMed  Google Scholar 

  251. Hong SI, Kang S, Chen JF, Choi DS. Indirect medium spiny neurons in the dorsomedial striatum regulate ethanol-containing conditioned reward seeking. J Neurosci. 2019;39:7206.

    Article  PubMed  PubMed Central  Google Scholar 

  252. Chow BY, Han X, Dobry AS, Qian X, Chuong AS, Li M, et al. High-performance genetically targetable optical neural silencing by light-driven proton pumps. Nature. 2010;463:98–102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Rost BR, Schneider-Warme F, Schmitz D, Hegemann P. Optogenetic tools for subcellular applications in neuroscience. Neuron. 2017;96:572–603.

    Article  CAS  PubMed  Google Scholar 

  254. Tye KM, Prakash R, Kim SY, Fenno LE, Grosenick L, Zarabi H, et al. Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature. 2011;471:358–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  255. Carter ME, Yizhar O, Chikahisa S, Nguyen H, Adamantidis A, Nishino S, et al. Tuning arousal with optogenetic modulation of locus coeruleus neurons. Nat Neurosci. 2010;13:1526–33.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Kravitz AV, Tye LD, Kreitzer AC. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci. 2012;15:816–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  257. Wentz CT, Oettl LL, Kelsch W. Optogenetics in psychiatric animal models. Cell Tissue Res. 2013;354(1):61–8.

    Article  CAS  PubMed  Google Scholar 

  258. Leopold AV, Shcherbakova DM, Verkhusha VV. Fluorescent biosensors for neurotransmission and neuromodulation: engineering and applications. Front Cell Neurosci. 2019;13:474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  259. Patriarchi T, Cho JR, Merten K, Howe MW, Marley A, Xiong WH, et al. Ultrafast neuronal imaging of dopamine dynamics with designed genetically encoded sensors. Science [Internet]. 2018 [cited 2022 June 19];360(6396):eaat4422. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6287765/.

  260. Mohebi A, Pettibone JR, Hamid AA, Wong JMT, Vinson LT, Patriarchi T, et al. Dissociable dopamine dynamics for learning and motivation. Nature. 2019;570:65–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  261. Sternson SM, Roth BL. Chemogenetic tools to interrogate brain functions. Annu Rev Neurosci. 2014;37:387–407.

    Article  CAS  PubMed  Google Scholar 

  262. Urban DJ, Roth BL. DREADDs (designer receptors exclusively activated by designer drugs): chemogenetic tools with therapeutic utility. Annu Rev Pharmacol Toxicol. 2015;55:399–417.

    Article  CAS  PubMed  Google Scholar 

  263. Armbruster BN, Li X, Pausch MH, Herlitze S, Roth BL. Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand. Proc Natl Acad Sci U S A. 2007;104(12):5163–8.

    Article  PubMed  PubMed Central  Google Scholar 

  264. Alexander GM, Rogan SC, Abbas AI, Armbruster BN, Pei Y, Allen JA, et al. Remote control of neuronal activity in transgenic mice expressing evolved G protein-coupled receptors. Neuron. 2009;63:27–39.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  265. Pati S, Saba K, Salvi SS, Tiwari P, Chaudhari PR, Verma V, et al. Chronic postnatal chemogenetic activation of forebrain excitatory neurons evokes persistent changes in mood behavior. Cheer JF, Wassum KM, Bolton J, Eisch AJ, editors. elife. 2020;9:e56171–1.

    Google Scholar 

  266. Mank M, Griesbeck O. Genetically encoded calcium indicators. Chem Rev. 2008;108:1550–64.

    Article  CAS  PubMed  Google Scholar 

  267. Nakai J, Ohkura M, Imoto K. A high signal-to-noise Ca2+ probe composed of a single green fluorescent protein. Nat Biotechnol. 2001;19:137–41.

    Article  CAS  PubMed  Google Scholar 

  268. Ohkura M, Matsuzaki M, Kasai H, Imoto K, Nakai J. Genetically encoded bright Ca2+ probe applicable for dynamic Ca2+ imaging of dendritic spines. Anal Chem. 2005;77:5861–9.

    Article  CAS  PubMed  Google Scholar 

  269. Sato M, Kawano M, Ohkura M, Gengyo-Ando K, Nakai J, Hayashi Y. Generation and imaging of transgenic mice that express G-CaMP7 under a tetracycline response element. PLoS One. 2015;10:e0125354.

    Article  PubMed  PubMed Central  Google Scholar 

  270. Chen X, Sobczak F, Chen Y, Jiang Y, Qian C, Lu Z, et al. Mapping optogenetically-driven single-vessel fMRI with concurrent neuronal calcium recordings in the rat hippocampus. Nat Commun. 2019;10:1–12.

    Article  Google Scholar 

  271. Cramer JV, Gesierich B, Roth S, Dichgans M, Düring M, Liesz A. In vivo widefield calcium imaging of the mouse cortex for analysis of network connectivity in health and brain disease. NeuroImage. 2019;199:570–84.

    Article  CAS  PubMed  Google Scholar 

  272. Alexandrov V, Brunner D, Hanania T, Leahy E. High-throughput analysis of behavior for drug discovery. Eur J Pharmacol. 2015;750:82–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  273. Brunner D, Nestler E, Leahy E. In need of high-throughput behavioral systems. Drug Discov Today. 2002;7(18 Suppl):S107–12.

    Article  CAS  PubMed  Google Scholar 

  274. Dedic N, Jones PG, Hopkins SC, Lew R, Shao L, Campbell JE, et al. SEP-363856, a novel psychotropic agent with a unique, non-D 2 receptor mechanism of action. J Pharmacol Exp Ther. 2019;371:1–14.

    Article  CAS  PubMed  Google Scholar 

  275. Koblan KS, Kent J, Hopkins SC, Krystal JH, Cheng H, Goldman R, et al. A non-D2-receptor-binding drug for the treatment of schizophrenia. N Engl J Med. 2020;382:1497–506.

    Article  CAS  PubMed  Google Scholar 

  276. Seligman MEP. Learned helplessness. Annu Rev Med. 1972;23:407–12.

    Article  CAS  PubMed  Google Scholar 

  277. Katz RJ, Roth KA, Carroll BJ. Acute and chronic stress effects on open field activity in the rat: implications for a model of depression. Neurosci Biobehav Rev. 1981;5:247–51.

    Article  CAS  PubMed  Google Scholar 

  278. Crema L, Schlabitz M, Tagliari B, Cunha A, Simão F, Krolow R, et al. Na+, K+ ATPase activity is reduced in amygdala of rats with chronic stress-induced anxiety-like behavior. Neurochem Res. 2010;35:1787–95.

    Article  CAS  PubMed  Google Scholar 

  279. Qi G, Zhang P, Li T, Li M, Zhang Q, He F, et al. NAc-VTA circuit underlies emotional stress-induced anxiety-like behavior in the three-chamber vicarious social defeat stress mouse model. Nat Commun. 2022;13:1–19.

    Article  Google Scholar 

  280. Pinna G, Agis-Balboa RC, Zhubi A, Matsumoto K, Grayson DR, Costa E, et al. Imidazenil and diazepam increase locomotor activity in mice exposed to protracted social isolation. Proc Natl Acad Sci U S A. 2006;103:4275–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Mumtaz F, Khan MI, Zubair M, Dehpour AR. Neurobiology and consequences of social isolation stress in animal model- a comprehensive review. Biomed Pharmacother. 2018;105:1205–22.

    Article  CAS  PubMed  Google Scholar 

  282. Rilke O, Will K, Jähkel M, Oehler J. Behavioral and neurochemical effects of anpirtoline and citalopram in isolated and group housed mice. Prog Neuro-Psychopharmacol Biol Psychiatry. 2001;25:1125–44.

    Article  CAS  Google Scholar 

  283. Petty F, Chae Y, lae, Kramer G, Jordan S, Wilson LA. Learned helplessness sensitizes hippocampal norepinephrine to mild restress. Biol Psychiatry. 1994;35:903–8.

    Article  CAS  PubMed  Google Scholar 

  284. Su CL, Su CW, Hsiao YH, Gean PW. Epigenetic regulation of BDNF in the learned helplessness-induced animal model of depression. J Psychiatr Res. 2016;76:101–10.

    Article  PubMed  Google Scholar 

  285. Sekine Y, Suzuki K, Ramachandran PV, Blackburn TP, Ashby CR. Acute and repeated administration of fluoxetine, citalopram, and paroxetine significantly alters the activity of midbrain dopamine neurons in rats: an in vivo electrophysiological study. Synapse. 2007;61:72–7.

    Article  CAS  PubMed  Google Scholar 

  286. Schwienteck KL, Li G, Poe MM, Cook JM, Banks ML, Negus S, S. Abuse-related effects of subtype-selective GABA A receptor positive allosteric modulators in an assay of intracranial self-stimulation in rats. Psychopharmacology. 2017;234:2091–101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  287. Vogel G, Neill D, Hagler M, Kors D, Hartley P. Decreased intracranial self-stimulation in a new animal model of endogenous depression. Neurosci Biobehav Rev. 1990;14:65–8.

    Article  CAS  PubMed  Google Scholar 

  288. Park J, Bucher ES, Fontillas K, Owesson-White C, Ariansen JL, Carelli RM, et al. Opposing catecholamine changes in the bed nucleus of the stria terminalis during intracranial self-stimulation and its extinction. Biol Psychiatry. 2013;74:69–76.

    Article  CAS  PubMed  Google Scholar 

  289. Ye Y, Yao S, Wang R, Fang Z, Zhong K, Nie L, et al. PI3K/Akt/NF-κB signaling pathway regulates behaviors in adolescent female rats following with neonatal maternal deprivation and chronic mild stress. Behav Brain Res. 2019;362:199–207.

    Article  CAS  PubMed  Google Scholar 

  290. Bourke CH, Stowe ZN, Neigh GN, Olson DE, Owens MJ. Prenatal exposure to escitalopram and/or stress in rats produces limited effects on endocrine, behavioral, or gene expression measures in adult male rats. Neurotoxicol Teratol. 2013;39:100–9.

    Article  CAS  PubMed  Google Scholar 

  291. Ramanathan M, Ashok Kumar SN, Suresh B. Evaluation of cognitive function of fluoxetine, sertraline and tianeptine in isolation and chronic unpredictable mild stress-induced depressive Wistar rats - PubMed. Indian J Exp Biol. 2003;41:1269–72.

    CAS  PubMed  Google Scholar 

  292. Chiba S, Numakawa T, Ninomiya M, Richards MC, Wakabayashi C, Kunugi H. Chronic restraint stress causes anxiety- and depression-like behaviors, downregulates glucocorticoid receptor expression, and attenuates glutamate release induced by brain-derived neurotrophic factor in the prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry. 2012;39:112–9.

    Article  CAS  PubMed  Google Scholar 

  293. McKlveen JM, Myers B, Flak JN, Bundzikova J, Solomon MB, Seroogy KB, et al. Role of prefrontal cortex glucocorticoid receptors in stress and emotion. Biol Psychiatry. 2013;74:672–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  294. Skelly MJ, Chappell AE, Carter E, Weiner JL. Adolescent social isolation increases anxiety-like behavior and ethanol intake and impairs fear extinction in adulthood: possible role of disrupted noradrenergic signaling. Neuropharmacology. 2015;97:149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  295. Barnes TD, Rieger MA, Dougherty JD, Holy TE. Group and individual variability in mouse pup isolation calls recorded on the same day show stability. Front Behav Neurosci. 2017;11:243.

    Article  PubMed  PubMed Central  Google Scholar 

  296. Huang Q, Zhou Y, Liu LY. Effect of post-weaning isolation on anxiety- and depressive-like behaviors of C57BL/6J mice. Exp Brain Res. 2017;235:2893–9.

    Article  PubMed  Google Scholar 

  297. Yorgason JT, España RA, Konstantopoulos JK, Weiner JL, Jones SR. Enduring increases in anxiety-like behavior and rapid nucleus accumbens dopamine signaling in socially isolated rats. Eur J Neurosci. 2013;37:1022–31.

    Article  PubMed  Google Scholar 

  298. Galea LAM, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS. Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience. 1997;81:689–97.

    Article  CAS  PubMed  Google Scholar 

  299. Pellow S, Chopin P, File SE, Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985;14:149–67.

    Article  CAS  PubMed  Google Scholar 

  300. Prut L, Belzung C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol. 2003;463:3–33.

    Article  CAS  PubMed  Google Scholar 

  301. Hall C, Ballachey EL. A study of the rat’s behavior in a field. A contribution to method in comparative psychology. Univ Calif Publ Psychol. 1932;6:1–12.

    Google Scholar 

  302. Xu Y, Ma L, Jiang W, Li Y, Wang G, Li R. Study of sex differences in duloxetine efficacy for depression in transgenic mouse models. Front Cell Neurosci. 2017;11:344.

    Article  PubMed  PubMed Central  Google Scholar 

  303. Flores-Ramirez FJ, Themann A, Sierra-Fonseca JA, Garcia-Carachure I, Castillo SA, Rodriguez M, et al. Adolescent fluoxetine treatment mediates a persistent anxiety-like outcome in female C57BL/6 mice that is ameliorated by fluoxetine re-exposure in adulthood. Sci Rep. 2021;11:7758.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  304. Wu YP, Gao HY, Ouyang SH, Kurihara H, He RR, Li YF. Predator stress-induced depression is associated with inhibition of hippocampal neurogenesis in adult male mice. Neural Regen Res. 2019;14:298–305.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  305. Wang H, Zuo D, He B, Qiao F, Zhao M, Wu Y. Conditioned fear stress combined with single-prolonged stress: a new PTSD mouse model. Neurosci Res. 2012;73:142–52.

    Article  PubMed  Google Scholar 

  306. Xu JN, Chen LF, Su J, Liu ZL, Chen J, Lin QF, et al. The anxiolytic-like effects of estazolam on a PTSD animal model. Psychiatry Res. 2018;269:529–35.

    Article  CAS  PubMed  Google Scholar 

  307. Piggott VM, Bosse KE, Lisieski MJ, Strader JA, Stanley JA, Conti AC, et al. Single-prolonged stress impairs prefrontal cortex control of amygdala and striatum in rats. Front Behav Neurosci. 2019;13:18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  308. Nedelcovych MT, Gould RW, Zhan X, Bubser M, Gong X, Grannan M, et al. A rodent model of traumatic stress induces lasting sleep and quantitative electroencephalographic disturbances. ACS Chem Neurosci. 2015;6:485–93.

    Article  CAS  PubMed  Google Scholar 

  309. Kvetňanský R, Mikulaj L. Adrenal and urinary catecholamines in rats during adaptation to repeated immobilization stress. Endocrinology. 1970;87:738–43.

    Article  PubMed  Google Scholar 

  310. van der Kolk B, Greenberg M, Boyd H, Krystal J. Inescapable shock, neurotransmitters, and addiction to trauma: toward a psychobiology of post traumatic stress. Biol Psychiatry. 1985;20:314–25.

    Article  PubMed  Google Scholar 

  311. Verbitsky A, Dopfel D, Zhang N. Rodent models of post-traumatic stress disorder: behavioral assessment. Transl Psychiatry. 2020;10:132.

    Article  PubMed  PubMed Central  Google Scholar 

  312. Berton O, McClung CA, DiLeone RJ, Krishnan V, Renthal W, Russo SJ, et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science (1979). 2006;311:864–8.

    CAS  Google Scholar 

  313. Gellhorn E. Interruption of behavior, inescapable shock, and experimental neurosis: a neurophysiologic analysis. Cond Reflex. 1967;2:285–93.

    Article  Google Scholar 

  314. Bentefour Y, Bennis M, Garcia R, M’Hamed SB. Effects of paroxetine on PTSD-like symptoms in mice. Psychopharmacology. 2015;232:2303–12.

    Article  CAS  PubMed  Google Scholar 

  315. Dahlhoff M, Siegmund A, Golub Y, Wolf E, Holsboer F, Wotjak CT. AKT/GSK-3beta/beta-catenin signalling within hippocampus and amygdala reflects genetically determined differences in posttraumatic stress disorder like symptoms. Neuroscience. 2010;169:1216–26.

    Article  CAS  PubMed  Google Scholar 

  316. Gao J, Wang H, Liu Y, Li YY, Chen C, Liu LM, et al. Glutamate and GABA imbalance promotes neuronal apoptosis in hippocampus after stress. Med Sci Monit. 2014;20:499–512.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  317. Adamec RE, Shallow T. Lasting effects on rodent anxiety of a single exposure to a cat. Physiol Behav. 1993;54:101–9.

    Article  CAS  PubMed  Google Scholar 

  318. Brad Wilson C, McLaughlin LD, Ebenezer PJ, Nair AR, Dange R, Harre JG, et al. Differential effects of sertraline in a predator exposure animal model of post-traumatic stress disorder. Front Behav Neurosci. 2014;8:256.

    PubMed  PubMed Central  Google Scholar 

  319. Wilson CB, Ebenezer PJ, McLaughlin LD, Francis J. Predator exposure/psychosocial stress animal model of post-traumatic stress disorder modulates neurotransmitters in the rat hippocampus and prefrontal cortex. PLoS One. 2014;9:e89104.

    Article  PubMed  PubMed Central  Google Scholar 

  320. Goswami S, Rodríguez-Sierra O, Cascardi M, Paré D. Animal models of post-traumatic stress disorder: face validity. Front Neurosci. 2013;7:89.

    Article  PubMed  PubMed Central  Google Scholar 

  321. Bourin M, Hascoët M. The mouse light/dark box test. Eur J Pharmacol. 2003;463:55–65.

    Article  CAS  PubMed  Google Scholar 

  322. Eagle AL, Fitzpatrick CJ, Perrine SA. Single prolonged stress impairs social and object novelty recognition in rats. Behav Brain Res. 2013;256:591–7.

    Article  PubMed  Google Scholar 

  323. Cohen SJ, Stackman RW. Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behav Brain Res. 2015;285:105–17.

    Article  PubMed  Google Scholar 

  324. Philbert J, Beeské S, Belzung C, Griebel G. The CRF1 receptor antagonist SSR125543 prevents stress-induced long-lasting sleep disturbances in a mouse model of PTSD: comparison with paroxetine and d-cycloserine. Behav Brain Res. 2015;279:41–6.

    Article  CAS  PubMed  Google Scholar 

  325. Shadli SM, Ando LC, McIntosh J, Lodhia V, Russell BR, Kirk IJ, et al. Right frontal anxiolytic-sensitive EEG ‘theta’ rhythm in the stop-signal task is a theory-based anxiety disorder biomarker. Sci Rep. 2021;11:1–12.

    Article  Google Scholar 

  326. McKillop LE, Fisher SP, Milinski L, Krone LB, Vyazovskiy VV. Diazepam effects on local cortical neural activity during sleep in mice. Biochem Pharmacol. 2021;191:114515.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  327. Troakes C, Ingram CD. Anxiety behaviour of the male rat on the elevated plus maze: associated regional increase in c-fos mRNA expression and modulation by early maternal separation. Stress. 2009;12:362–9.

    Article  CAS  PubMed  Google Scholar 

  328. Badiani A, Oates MM, Day HEW, Watson SJ, Akil H, Robinson TE. Amphetamine-induced behavior, dopamine release, and c-fos mRNA expression: modulation by environmental novelty. J Neurosci. 1998;18:10579–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  329. Cochran SM, Kennedy M, McKerchar CE, Steward LJ, Pratt JA, Morris BJ. Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology. 2003;28:265–75.

    Article  CAS  PubMed  Google Scholar 

  330. Lipska BK, Weinberger DR. Delayed effects of neonatal hippocampal damage on haloperidol-induced catalepsy and apomorphine-induced stereotypic behaviors in the rat. Brain Res Dev Brain Res. 1993;75:213–22.

    Article  CAS  PubMed  Google Scholar 

  331. Lipska BK, Weinberger DR. Subchronic treatment with haloperidol and clozapine in rats with neonatal excitotoxic hippocampal damage. Neuropsychopharmacology. 1994;10:199–205.

    Article  CAS  PubMed  Google Scholar 

  332. Lipska BK, Lerman DN, Khaing ZZ, Weickert CS, Weinberger DR. Gene expression in dopamine and GABA systems in an animal model of schizophrenia: effects of antipsychotic drugs. Eur J Neurosci. 2003;18:391–402.

    Article  PubMed  Google Scholar 

  333. Le Pen G, Moreau JL. Disruption of prepulse inhibition of startle reflex in a neurodevelopmental model of schizophrenia: reversal by clozapine, olanzapine and risperidone but not by haloperidol. Neuropsychopharmacology. 2002;27:1–11.

    Article  PubMed  Google Scholar 

  334. O’Donnell P. Cortical disinhibition in the neonatal ventral hippocampal lesion model of schizophrenia: new vistas on possible therapeutic approaches. Pharmacol Ther. 2012;133:19–25.

    Article  PubMed  Google Scholar 

  335. Fiore M, Di Fausto V, Aloe L. Clozapine or haloperidol in rats prenatally exposed to methylazoxymethanol, a compound inducing entorhinal-hippocampal deficits, alter brain and blood neurotrophins’ concentrations - PubMed. Ann Ist Super Sanita. 2008;44:167–77.

    CAS  PubMed  Google Scholar 

  336. Lavin A, Moore HM, Grace AA. Prenatal disruption of neocortical development alters prefrontal cortical neuron responses to dopamine in adult rats. Neuropsychopharmacology. 2005;30:1426–35.

    Article  CAS  PubMed  Google Scholar 

  337. Lodge DJ, Behrens MM, Grace AA. A loss of parvalbumin-containing interneurons is associated with diminished oscillatory activity in an animal model of schizophrenia. J Neurosci. 2009;29:2344–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  338. Stevens KE, Johnson RG, Rose GM. Rats reared in social isolation show schizophrenia-like changes in auditory gating. Pharmacol Biochem Behav. 1997;58:1031–6.

    Article  CAS  PubMed  Google Scholar 

  339. Lapiz MD, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA. Influence of postweaning social isolation in the rat on brain development, conditioned behaviour and neurotransmission. Rossiiskii fiziologicheskii zhurnal imeni IM Sechenova/Rossiĭskaia akademiia nauk. 2001;87:730–51.

    CAS  Google Scholar 

  340. Fone KCF, Porkess MV. Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev. 2008;32:1087–102.

    Article  CAS  PubMed  Google Scholar 

  341. Heidbreder CA, Foxton R, Cilia J, Hughes ZA, Shah AJ, Atkins A, et al. Increased responsiveness of dopamine to atypical, but not typical antipsychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology. 2001;156:338–51.

    Article  CAS  PubMed  Google Scholar 

  342. Karayiorgou M, Morris MA, Morrow B, Shprintzen RJ, Goldberg R, Borrow J, et al. Schizophrenia susceptibility associated with interstitial deletions of chromosome 22q11. Proc Natl Acad Sci U S A. 1995;92:7612–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  343. Xu B, Roos JL, Levy S, Van Rensburg EJ, Gogos JA, Karayiorgou M. Strong association of de novo copy number mutations with sporadic schizophrenia. Nat Genet. 2008;40:880–5.

    Article  CAS  PubMed  Google Scholar 

  344. Campbell LE, Daly E, Toal F, Stevens A, Azuma R, Catani M, et al. Brain and behaviour in children with 22q11.2 deletion syndrome: a volumetric and voxel-based morphometry MRI study. Brain. 2006;129:1218–28.

    Article  PubMed  Google Scholar 

  345. Simon TJ, Bish JP, Bearden CE, Ding L, Ferrante S, Nguyen V, et al. A multilevel analysis of cognitive dysfunction and psychopathology associated with chromosome 22q11.2 deletion syndrome in children. Dev Psychopathol. 2005;17:753–84.

    Article  PubMed  PubMed Central  Google Scholar 

  346. Gothelf D, Law AJ, Frisch A, Chen J, Zarchi O, Michaelovsky E, et al. Biological effects of COMT haplotypes and psychosis risk in 22q11.2 deletion syndrome. Biol Psychiatry. 2014;75:406–13.

    Article  CAS  PubMed  Google Scholar 

  347. Didriksen M, Fejgin K, Nilsson SRO, Birknow MR, Grayton HM, Larsen PH, et al. Persistent gating deficit and increased sensitivity to NMDA receptor antagonism after puberty in a new mouse model of the human 22q11.2 microdeletion syndrome: a study in male mice. J Psychiatry Neurosci. 2017;42:48–58.

    Article  PubMed  Google Scholar 

  348. Tripathi A, Spedding M, Schenker E, Didriksen M, Cressant A, Jay TM. Cognition- and circuit-based dysfunction in a mouse model of 22q11.2 microdeletion syndrome: effects of stress. Transl Psychiatry. 2020;10:1–15.

    Article  Google Scholar 

  349. Hodgkinson CA, Goldman D, Jaeger J, Persaud S, Kane JM, Lipsky RH, et al. Disrupted in schizophrenia 1 (DISC1): association with schizophrenia, schizoaffective disorder, and bipolar disorder. Am J Hum Genet. 2004;75:862–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  350. Kamiya A, Kubo KI, Tomoda T, Takaki M, Youn R, Ozeki Y, et al. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat Cell Biol. 2005;7:1067–78.

    Article  CAS  Google Scholar 

  351. Niwa M, Kamiya A, Murai R, Kubo K, Gruber AJ, Tomita K, et al. Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron. 2010;65:480–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  352. Andersen MP, Pouzet B. Effects of acute versus chronic treatment with typical or atypical antipsychotics on d-amphetamine-induced sensorimotor gating deficits in rats. Psychopharmacology. 2001;156:291–304.

    Article  CAS  PubMed  Google Scholar 

  353. Mavrikaki M, Nomikos GG, Panagis G. Efficacy of the atypical antipsychotic aripiprazole in d-amphetamine-based preclinical models of mania. Int J Neuropsychopharmacol. 2010;13:541–8.

    Article  CAS  PubMed  Google Scholar 

  354. Kitaichi K, Yamada K, Hasegawa T, Nabeshima T, Furukawa H. Effects of risperidone on phencyclidine-induced behaviors: comparison with haloperidol and ritanserin. Jpn J Pharmacol. 1994;66:181–9.

    Article  CAS  PubMed  Google Scholar 

  355. Hoffman DC. Typical and atypical neuroleptics antagonize MK-801-induced locomotion and stereotypy in rats. J Neural Transm Gen Sect. 1992;89:1–10.

    Article  CAS  PubMed  Google Scholar 

  356. Minnaard AM, Ramakers GMJ, Vanderschuren LJMJ, Lesscher HMB. Baclofen and naltrexone, but not N-acetylcysteine, affect voluntary alcohol drinking in rats regardless of individual levels of alcohol intake. Behav Pharmacol. 2021;32:251–7.

    Article  CAS  PubMed  Google Scholar 

  357. Mello NK, Negus SS. Preclinical evaluation of pharmacotherapies for treatment of cocaine and opioid abuse using drug self-administration procedures. Neuropsychopharmacology. 1996;14:375.

    Article  CAS  PubMed  Google Scholar 

  358. Weeks JR. Experimental morphine addiction: method for automatic intravenous injections in unrestrained rats. Science. 1979;1962(138):143–4.

    Google Scholar 

  359. Leri F, Tremblay A, Sorge RE, Stewart J. Methadone maintenance reduces heroin- and cocaine-induced relapse without affecting stress-induced relapse in a rodent model of poly-drug use. Neuropsychopharmacology. 2004;29:1312–20.

    Article  CAS  PubMed  Google Scholar 

  360. Mello NK, Mendelson JH, Bree MP, Lukas SE. Buprenorphine and naltrexone effects on cocaine self-administration by rhesus monkeys. J Pharmacol Exp Ther. 1990;254:926–39.

    CAS  PubMed  Google Scholar 

  361. Mello NK, Lukas SE, Mendelson JH, Drieze J. Naltrexone–buprenorphine interactions: effects on cocaine self-administration. Neuropsychopharmacology. 1993;9:211–24.

    Article  CAS  PubMed  Google Scholar 

  362. Jordan CJ, Cao J, Newman AH, Xi ZX. Progress in agonist therapy for substance use disorders: lessons learned from methadone and buprenorphine. Neuropharmacology. 2019;158:107609.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  363. Beach HD. Morphine addiction in rats. Can J Psychol. 1957;11:104–12.

    Article  CAS  PubMed  Google Scholar 

  364. Bespalov AY, Tokarz ME, Bowen SE, Balster RL, Bear. Effects of test conditions on the outcome of place conditioning with morphine and naltrexone in mice. Psychopharmacology. 1999;141:118–22.

    Article  CAS  PubMed  Google Scholar 

  365. Houj M, Bisaga A, Popik P. Conditioned rewarding effects of morphine and methadone in mice pre-exposed to cocaine. Pharmacol Rep. 2013;65:1176–84.

    Article  Google Scholar 

  366. Myers MM, Musty RE, Hendley ED. Attenuation of hyperactivity in the spontaneously hypertensive rat by amphetamine. Behav Neural Biol. 1982;34:42–54.

    Article  CAS  PubMed  Google Scholar 

  367. Sagvolden T. The alpha-2A adrenoceptor agonist guanfacine improves sustained attention and reduces overactivity and impulsiveness in an animal model of attention-deficit/hyperactivity disorder (ADHD). Behav Brain Funct. 2006;2:41.

    Article  PubMed  PubMed Central  Google Scholar 

  368. Miller EM, Pomerleau F, Huettl P, Russell VA, Gerhardt GA, Glaser PEA. The spontaneously hypertensive and Wistar Kyoto rat models of ADHD exhibit sub-regional differences in dopamine release and uptake in the striatum and nucleus accumbens. Neuropharmacology. 2012;63:1327–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  369. Zhuang X, Oosting RS, Jones SR, Gainetdinov RR, Miller GW, Caron MG, et al. Hyperactivity and impaired response habituation in hyperdopaminergic mice. Proc Natl Acad Sci U S A. 2001;98:1982–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  370. Hardung S, Jäckel Z, Diester I. Prefrontal contributions to action control in rodents. Int Rev Neurobiol. 2021;158:373–93.

    Article  PubMed  Google Scholar 

  371. Moon SJ, Kim CJ, Lee YJ, Hong M, Han J, Bahn GH. Effect of atomoxetine on hyperactivity in an animal model of attention-deficit/hyperactivity disorder (ADHD). PLoS One. 2014;9:e108918.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Author notes

  1. Laura B. Teal, Shalonda M. Ingram and Carrie K. Jones contributed equally to this work.

Authors and Affiliations

  1. Department of Pharmacology, Vanderbilt University, Nashville, TN, USA

    Laura B. Teal, Shalonda M. Ingram, Michael Bubser & Carrie K. Jones

  2. Warren Center for Neuroscience Drug Discovery, Vanderbilt University, Nashville, TN, USA

    Laura B. Teal, Shalonda M. Ingram, Michael Bubser & Carrie K. Jones

  3. College of Pharmacy and Health Sciences, Lipscomb University, Nashville, TN, USA

    Elliott McClure

Authors
  1. Laura B. Teal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shalonda M. Ingram
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael Bubser
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elliott McClure
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carrie K. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Carrie K. Jones .

Editor information

Editors and Affiliations

  1. Department of Psychiatry and Behavioral Neurobiology, University of Alabama at Birmingham Heersink School of Medicine, Birmingham, AL, USA

    Matthew Macaluso

  2. Department of Psychiatry and Behavioral Science, Kansas University School of Medicine-Wichita campus, Wichita, KS, USA

    Sheldon H. Preskorn

  3. Department of Psychiatry and Behavioral Neurobiology, University of Alabama at Birmingham Heersink School of Medicine, Birmingham, AL, USA

    Richard C. Shelton

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Teal, L.B., Ingram, S.M., Bubser, M., McClure, E., Jones, C.K. (2023). The Evolving Role of Animal Models in the Discovery and Development of Novel Treatments for Psychiatric Disorders. In: Macaluso, M., Preskorn, S.H., Shelton, R.C. (eds) Drug Development in Psychiatry. Advances in Neurobiology, vol 30. Springer, Cham. https://doi.org/10.1007/978-3-031-21054-9_3

Download citation

Publish with us

Policies and ethics

Search

Navigation