Abstract
Grooming is a commonplace, robust behavior in rodent species. It has been shown to be highly sensitive to a number of experimental factors, making it an ideal target for manipulation. The complex patterning of grooming in rodents, which usually proceeds in a cephalo-caudal direction and involves several distinct stages, can be dissected into its constituent parts and microstructures. Several grooming patterning analysis methods are described in the protocol that allow for an assessment of this behavior based on measurements of grooming activity and its sequencing. Additionally, grooming can be evaluated in reference to the regional distribution and syntax in which it occurs. Owing to the ever-increasing number of rodent models that have strong grooming phenotypes, this high-throughput in-depth analysis is becoming crucial for biomedical research.
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References
Bolles, R.C. Grooming behavior in the rat. J. Comp. Physiol. Psychol. 53, 306–310 (1960).
Spruijt, B.M., van Hooff, J.A. & Gispen, W.H. Ethology and neurobiology of grooming behavior. Physiol. Rev. 72, 825–852 (1992).
Kalueff, A.V. & Tuohimaa, P. Contrasting grooming phenotypes in C57Bl/6 and 129S1/SvImJ mice. Brain Res. 1028, 75–82 (2004).
Kalueff, A.V. & Tuohimaa, P. Grooming analysis algorithm for neurobehavioural stress research. Brain Res. 13, 151–158 (2004).
Spencer, S.J., Mouihate, A. & Pittman, Q.J. Peripheral inflammation exacerbates damage after global ischemia independently of temperature and acute brain inflammation. Stroke 38, 1570–1577 (2007).
Qi, X., Lin, W., Li, J., Pan, Y. & Wang, W. The depressive-like behaviors are correlated with decreased phosphorylation of mitogen-activated protein kinases in rat brain following chronic forced swim stress. Behav. Brain Res. 175, 233–240 (2006).
McFarlane, H.G. et al. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. (in the press).
Kalueff, A.V., Lou, Y.R., Laaksi, I. & Tuohimaa, P. Increased grooming behavior in mice lacking vitamin D receptors. Physiol. Behav. 82, 405–409 (2004).
Kallnik, M. et al. Impact of IVC housing on emotionality and fear learning in male C3HeB/FeJ and C57BL/6J mice. Mamm. Genome 18, 173–186 (2007).
Pekcec, A., Muhlenhoff, M., Gerardy-Schahn, R. & Potschka, H. Impact of the PSA-NCAM system on pathophysiology in a chronic rodent model of temporal lobe epilepsy. Neurobiol. Dis. 27, 54–66 (2007).
Spruijt, B.M., De Graan, P.N., Eberle, A.N. & Gispen, W.H. Comparison of structural requirements of alpha-MSH and ACTH for inducing excessive grooming and pigment dispersion. Peptides 6, 1185–1189 (1985).
Spruijt, B.M., Welbergen, P., Brakkee, J. & Gispen, W.H. Behavioral changes in ACTH-(1-24)-induced excessive grooming in aging rats. Neurobiol. Aging 8, 265–270 (1987).
Kalueff, A.V. & Tuohimaa, P. Mouse grooming microstructure is a reliable anxiety marker bidirectionally sensitive to GABAergic drugs. Eur. J. Pharmacol. 508, 147–153 (2005).
Crawley, J.N. & Moody, T.W. Anxiolytics block excessive grooming behavior induced by ACTH1-24 and bombesin. Brain Res. Bull. 10, 399–401 (1983).
Moody, T.W., Merali, Z. & Crawley, J.N. The effects of anxiolytics and other agents on rat grooming behavior. Ann. NY Acad. Sci. 525, 281–290 (1988).
Greer, J.M. & Capecchi, M.R. Hoxb8 is required for normal grooming behavior in mice. Neuron 33, 23–34 (2002).
Welch, M.J. et al. Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature 448, 894–900 (2007).
Yamamoto, T. & Ueki, S. Behavioral effects of 2,5-dimethoxy-4-methylamphetamine (DOM) in rats and mice. Eur. J. Pharmacol. 32, 156–162 (1975).
File, S.E., Mabbutt, P.S. & Walker, J.H. Comparison of adaptive responses in familiar and novel environments: modulatory factors. Ann. NY Acad. Sci. 525, 69–79 (1988).
Fentress, J.C. & Stilwell, F.P. Letter: grammar of a movement sequence in inbred mice. Nature 244, 52–53 (1973).
Fentress, J.C. Development of grooming in mice with amputated forelimbs. Science 179, 704–705 (1973).
Fentress, J.C. The tonic hypothesis and the patterning of behavior. Ann. NY Acad. Sci. 290, 370–395 (1977).
Berridge, K.C. & Fentress, J.C. Deafferentation does not disrupt natural rules of action syntax. Behav. Brain Res. 23, 69–76 (1987).
Berridge, K.C., Fentress, J.C. & Parr, H. Natural syntax rules control action sequence of rats. Behav. Brain Res. 23, 59–68 (1987).
Berridge, K.C. & Aldridge, J.W. Super-stereotypy II: enhancement of a complex movement sequence by intraventricular dopamine D1 agonists. Synapse 37, 205–215 (2000).
Berridge, K.C. & Aldridge, J.W. Super-stereotypy I: enhancement of a complex movement sequence by systemic dopamine D1 agonists. Synapse 37, 194–204 (2000).
Berridge, K.C., Aldridge, J.W., Houchard, K.R. & Zhuang, X. Sequential super-stereotypy of an instinctive fixed action pattern in hyper-dopaminergic mutant mice: a model of obsessive compulsive disorder and Tourette's. BMC Biol. 3, 4 (2005).
Audet, M.C., Goulet, S. & Dore, F.Y. Repeated subchronic exposure to phencyclidine elicits excessive atypical grooming in rats. Behav. Brain Res. 167, 103–110 (2006).
Komorowska, J. & Pellis, S.M. Regulatory mechanisms underlying novelty-induced grooming in the laboratory rat. Behav. Processes 67, 287–293 (2004).
Kobayashi, M. et al. Electrophysiological analysis of rhythmic jaw movements in the freely moving mouse. Physiol. Behav. 75, 377–385 (2002).
Matell, M.S., Berridge, K.C. & Wayne Aldridge, J. Dopamine D1 activation shortens the duration of phases in stereotyped grooming sequences. Behav. Processes 71, 241–249 (2006).
Kalueff, A.V. & Tuohimaa, P. The grooming analysis algorithm discriminates between different levels of anxiety in rats: potential utility for neurobehavioural stress research. J. Neurosci. Methods 143, 169–177 (2005).
Aldridge, J.W. & Berridge, K.C. Coding of serial order by neostriatal neurons: a 'natural action' approach to movement sequence. J. Neurosci. 18, 2777–2787 (1998).
Aldridge, J.W., Berridge, K.C. & Rosen, A.R. Basal ganglia neural mechanisms of natural movement sequences. Can. J. Physiol. Pharmacol. 82, 732–739 (2004).
Aldridge, J.W. Syntactic grooming in the rat and its neural mechanisms. in The Behaviour of the Laboratory Rat: A Handbook with Tests (eds. Whishaw, I. & Kolb, B.) 141–149 (MIT Press, Cambridge, MA, 2004).
Cromwell, H.C. & Berridge, K.C. Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J. Neurosci. 16, 3444–3458 (1996).
Berridge, K.C. Progressive degradation of serial grooming chains by descending decerebration. Behav. Brain Res. 33, 241–253 (1989).
Berridge, K.C. & Whishaw, I.Q. Cortex, striatum and cerebellum: control of serial order in a grooming sequence. Exp. Brain Res. 90, 275–290 (1992).
Cromwell, H.C., Berridge, K.C., Drago, J. & Levine, M.S. Action sequencing is impaired in D1A-deficient mutant mice. Eur. J. Neurosci. 10, 2426–2432 (1998).
Deacon, R.M. Housing, husbandry and handling of rodents for behavioral experiments. Nat. Protoc. 1, 936–946 (2006).
Kalueff, A.V. & Tuohimaa, P. Contrasting grooming phenotypes in three mouse strains markedly different in anxiety and activity (129S1, BALB/c and NMRI). Behav. Brain Res. 160, 1–10 (2005).
Burne, T.H., Johnston, A.N., McGrath, J.J. & Mackay-Sim, A. Swimming behaviour and post-swimming activity in vitamin D receptor knockout mice. Brain Res. Bull. 69, 74–78 (2006).
Dunn, A.J., Berridge, C.W., Lai, Y.I. & Yachabach, T.L. CRF-induced excessive grooming behavior in rats and mice. Peptides 8, 841–844 (1987).
Kalueff, A.V., Lou, Y.R., Laaksi, I. & Tuohimaa, P. Abnormal behavioral organization of grooming in mice lacking the vitamin D receptor gene. J. Neurogenet. 19, 1–24 (2005).
Molloy, A.G. & Waddington, J.L. Dopaminergic behaviour stereospecific promoted by the D1 agonist R-SK & F 38393 and selectively blocked by the D1 antagonist SCH 23390. Psychopharmacology 82, 409–410 (1984).
Molloy, A.G., Aronstam, R.S. & Buccafusco, J.J. Selective antagonism by clonidine of the stereotyped and non-stereotyped motor activity elicited by atropine. Pharmacol. Biochem. Behav. 25, 985–988 (1986).
Waddington, J.L., Molloy, A.G., O'Boyle, K.M. & Mashurano, M. Motor consequences of D-1 dopamine receptor stimulation and blockade. Clin. Neuropharmacol. 9 (suppl. 4): 20–22 (1986).
Molloy, A.G. & Waddington, J.L. Assessment of grooming and other behavioural responses to the D-1 dopamine receptor agonist SK & F 38393 and its R- and S-enantiomers in the intact adult rat. Psychopharmacology 92, 164–168 (1987).
Crawley, J.N. What's Wrong with My Mouse? Behavioral Phenotyping of Transgenic and Knockout Mice (Wiley-Liss, New York, NY, 2000).
Hill, R.A. et al. Estrogen deficient male mice develop compulsive behavior. Biol. Psychiatry 61, 359–366 (2007).
Wurbel, H. Ideal homes? Housing effects on rodent brain and behaviour. Trends Neurosci. 24, 207–211 (2001).
Wolfer, D.P. et al. Laboratory animal welfare: cage enrichment and mouse behaviour. Nature 432, 821–822 (2004).
Kalueff, A.V., Keisala, T., Minasyan, A. & Tuohimaa, P. Influence of paternal genotypes on F1 behaviors: lessons from several mouse strains. Behav. Brain Res. 177, 45–50 (2007).
Enginar, N., Hatipoglu, I. & Firtina, M. Evaluation of the effect of amitriptyline and fluoxetine on anxiety using the grooming analysis algorithm in rats. Proc. Stress Behav. Conf. 10, 18–19 (2007).
Spasojevic, N., Gavrilovic, L., Varagic, V.V. & Dronjak, S. Effects of chronic diazepam treatments on behavior of individually housed rats. Arch. Biol. Sci. 59, 113–117 (2007).
Kalueff, A.V., Wheaton, M. & Murphy, D.L. What's wrong with my mouse model? Advances and strategies in animal modeling of anxiety and depression. Behav. Brain Res. 179, 1–18 (2007).
Acknowledgements
This research was supported in part by the Medical Research Foundation (EVO) of Tampere University Hospital (Finland), the Intramural Research Program of the National Institute of Mental Health (USA) and NARSAD YI Award (to A.V.K.). We thank Professor Kent Berridge (University of Michigan, USA) for permission to use grooming syntax diagram and for his valuable comments on earlier versions of this manuscript.
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Supplementary Video 1
Non-chain rat grooming (MOV 214 kb)
Supplementary Video 2
Syntactic chain grooming in rats (Example 1) (MOV 508 kb)
Supplementary Video 3
Syntactic chain grooming in rats (Example 2) (MOV 574 kb)
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Kalueff, A., Aldridge, J., LaPorte, J. et al. Analyzing grooming microstructure in neurobehavioral experiments. Nat Protoc 2, 2538–2544 (2007). https://doi.org/10.1038/nprot.2007.367
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DOI: https://doi.org/10.1038/nprot.2007.367
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