Skip to main content
Log in

Dopaminergic Modulation of Spiny Neurons in the Turtle Striatum

  • Original Research
  • Published:
Cellular and Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Intracellular recordings were obtained from brain slice preparation in neurons of the striatum of the turtle Trachemys scripta elegans, analogous to the mammalian striatum in its topographic organization, synaptic connectivity, cytoarchitecture, and neurochemistry. Here we show that these similarities extend to the electrophysiological properties of its neurons. Biocytin staining revealed that 85% of the recorded neurons were medium spiny neurons while 15% were aspiny neurons. Spiny neurons of the turtle resembled those found in the mammalian and avian striatum and express dopaminergic D1 and D2 class receptors. Because the striatum of the turtle receives a dense dopaminergic innervation from tegmental dopaminergic neurons we investigated the postsynaptic actions of selective dopamine receptor agonists in the excitability of spiny neurons. As in mammals and birds, activation of D1-receptors enhances, whereas activation of D2-receptors decreases the evoked discharge. Apparently, actions of dopamine agonists occur via the modulation of L-type (CaV1) Ca2+-conductances. Strong cellular evidence suggests that the role of dopamine in the modulation of motor networks is preserved along vertebrate evolution.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Andersen A, Baestrup C, Randrup A (1975) Apomorphine-induced stereotyped biting in the tortoise in relation to dopaminergic mechanisms. Brain Behav Evol 11:365–373

    Article  CAS  PubMed  Google Scholar 

  • Bargas J, Galarraga E, Aceves J (1989) An early outward conductance modulates the firing latency and frequency of neostriatal neurons of the rat brain. Exp Brain Res 75:146–156

    Article  CAS  PubMed  Google Scholar 

  • Brauth SE, Reiner A, Kitt CA, Karten HJ (1983) The substance P-containing striato-tegmental path in reptiles: an immunohistochemical study. J Comp Neurol 219:305–327

    Article  CAS  PubMed  Google Scholar 

  • Butler A, Hodos W (2005). Comparative vertebrate neuroanatomy, evolution and adaptation, 2nd edn. Wiley Interscience, p 484

  • Carrillo-Reid L, Tecuapetla F, Tapia D, Hernandez-Cruz A, Galarraga E, Drucker-Colin R, Bargas J (2008) Encoding network states by striatal cell assemblies. J Neurophysiol 99:1435–1450

    Article  PubMed  Google Scholar 

  • Cepeda C, Colwell CS, Itri JN, Chandler SH, Levine MS (1998) Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J Neurophysiol 79:82–94

    CAS  PubMed  Google Scholar 

  • Delgado-Lezama R, Perrier JF, Hounsgaard J (1999) Oscillatory interaction between dorsal root excitability and dorsal root potentials in the spinal cord of the turtle. Neurosci 93:731–739

    Article  CAS  Google Scholar 

  • Ding L, Perkel DJ (2002) Dopamine modulates excitability of spiny neurons in the avian basal ganglia. J Neurosci 22:5210–5218

    CAS  PubMed  Google Scholar 

  • Donkelaar HJT (1998) Reptiles. In: Nieuwenhuys R, Donkeelar HJT, Nicholson C (eds) Central nervous system of vertebrates. Springer-Verlag, Berlin, pp 1315–1524

    Google Scholar 

  • Farries MA, Perkel DJ (2000) Electrophysiological properties of avian basal ganglia neurons recorded in vitro. J Neurophysiol 84:2502–2513

    CAS  PubMed  Google Scholar 

  • Farries MA, Perkel DJ (2002) A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both Striatum and Globus Pallidus. J Neurosci 22:3776–3787

    CAS  PubMed  Google Scholar 

  • Farries MA, Meitzen J, Perkel DJ (2005) Electrophysiological properties of neurons in the basal ganglia of the domestic chick: conservation and divergence in the evolution of the avian basal ganglia. J Neurophysiol 94:454–467

    Article  PubMed  Google Scholar 

  • Fowler M, Medina L, Reiner A (1999) Inmunohistochemical localization of NMDA- and AMPA-type glutamate receptor subunits in the basal ganglia of red eared turtles. Brain Behav Evol 54:276–289

    Article  CAS  PubMed  Google Scholar 

  • Galarraga E, Pacheco-Cano MT, Flores-Hernández JV, Bargas J (1994) Subthreshold rectification in neostriatal spiny projection neurons. Exp Brain Res 100:239–249

    Article  CAS  PubMed  Google Scholar 

  • Galarraga E, Hernández-López S, Reyes A, Barral J, Bargas J (1997) Dopamine facilitates EPSPs through an L-type Ca2+-conductance. Neuroreport 8:2183–2186

    Article  CAS  PubMed  Google Scholar 

  • González A, Smeets WJAJ (1994) Catecholamine systems in the CNS of amphibians. In: Smeets WJAJ, Reiner A (eds) Phylogeny and development of catecholamine systems in the CNS of vertebrates. Cambridge University Press, Cambridge, pp 77–102

    Google Scholar 

  • González-Burgos G, Kröner S, Krimer LS, Seamans JK, Urban NN, Henze DA, Lewis DA, Barrionuevo G (2002) Dopamine modulation of neuronal function in the monkey prefrontal cortex. Physiol Behav 77:537–543

    Article  PubMed  Google Scholar 

  • Graybiel AM (1990) The basal ganglia and the initiation of the movement. Rev Neurol 146:570–574

    CAS  PubMed  Google Scholar 

  • Greenberg N, Font E, Switzer RC (1988) The reptilian striatum revisited: studies on Anolis lizards. In: Schwerdtfeger WK, Smeets WJAJ (eds) The forebrain of reptiles: current concepts of structure, function. Karger, Basel, pp 162–177

    Google Scholar 

  • Grillner S (2006) Biological pattern generation: the cellular and computational logic of networks in motion. Neuron 52:751–766

    Article  CAS  PubMed  Google Scholar 

  • Guzmán JN, Hernandez A, Galarraga E, Tapia D, Laville A, Vergara R, Aceves J, Bargas J (2003) Dopaminergic modulation of axon collaterals interconnecting spiny neurons of the rat striatum. J Neurosci 23:8931–8940

    PubMed  Google Scholar 

  • Henselmans JM, Hoogland PV, Stoof JC (1991) Differences in the regulation of acetylcholine release upon D2 dopamine and N-methyl-D-aspartate receptor activation between the striatal complex of reptiles and the neostriatum of rats. Brain Res 566:8–12

    Article  CAS  PubMed  Google Scholar 

  • Henze DA, González-Burgos GR, Urban NN, Lewis DA, Barrionuevo G (2000) Dopamine increases excitability of pyramidal neurons in primate prefrontal cortex. J Neurophysiol 84:2799–2809

    CAS  PubMed  Google Scholar 

  • Hernández-López S, Bargas J, Surmeier DJ, Reyes A, Galarraga E (1997) D1 receptor activation enhances evoked discharge in neostriatal medium spiny neurons by modulating an L-type Ca2+-conductance. J Neurosci 17:3334–3342

    PubMed  Google Scholar 

  • Hernández-López S, Tkatch T, Pérez-Garci E, Galarraga E, Bargas J, Hamm H, Surmeier DJ (2000) D2 dopamine receptors in striatal medium spiny neurons reduce L-type Ca2+ currents and excitability through a novel PLCB1/IP3/calcineurin signaling cascade. J Neurosci 20:8987–8995

    PubMed  Google Scholar 

  • Hopf FW, Mailliard WS, Gonzalez GF, Diamond I, Bonci A (2005) Atypical protein kinase C is a novel mediator of dopamine-enhanced firing in nucleus accumbens neurons. J Neurosci 25:985–989

    Article  CAS  PubMed  Google Scholar 

  • Kröner S, Rosenkranz JA, Grace A, Barrionuevo G (2005) Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 93:1598–1610

    Article  PubMed  Google Scholar 

  • Lefebvre L, Reader SM, Sol D (2004) Brains, innovations and evolution in birds and primates. Brain Behav Evol 63:233–246

    Article  PubMed  Google Scholar 

  • Marin O, Smeets W, González A (1998) Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians. TINS 21:487–494

    CAS  PubMed  Google Scholar 

  • Medina L, Reiner A (1995) Neurotransmitter organization and connectivity of the basal ganglia in vertebrates: implications for the evolution of basal ganglia. Brain Behav Evol 46:235–258

    Article  CAS  PubMed  Google Scholar 

  • Medina L, Smeets WJAJ (1991) Comparative aspects of the basal ganglia-tectal pathways in reptiles. J Comp Neurol 308:614–629

    Article  CAS  PubMed  Google Scholar 

  • Nisenbaum ES, Wilson CJ (1995) Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J Neurosci 15:4449–4463

    CAS  PubMed  Google Scholar 

  • Northcutt RG (1981) Evolution of the telencephalon in non-mammals. Ann Rev Neurosci 4:301–350

    Article  CAS  PubMed  Google Scholar 

  • Pacheco-Cano MT, Bargas J, Hernández-López S, Tapia D, Galarraga E (1996) Inhibitory action of dopamine involves a subthreshold Cs+-sensitive conductance. Exp Brain Res 110:205–211

    Article  CAS  PubMed  Google Scholar 

  • Parent A (1973) Distribution of monoamine-containing nerve terminals in the brain of the painted turtle, Chrysemys picta. J Comp Neurol 148:153–165

    Article  CAS  PubMed  Google Scholar 

  • Parent A (1976) Striatal afferent connections in the turtle (Chrysemys picta) as revealed by retrograde axonal transport of horseradish peroxidase. Brain Res 108:25–36

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Garci E, Bargas J, Galarraga E (2003) The role of Ca2+ channels in the repetitive firing of striatal projection neurons. Neuroreport 14:1253–1256

    Article  PubMed  Google Scholar 

  • Perkel DJ, Farries MA (2000) Complementary ‘bottom-up’ and ‘top-down’ approaches to basal ganglia function. Curr Opin Neurobiol 10:725–731

    Article  CAS  PubMed  Google Scholar 

  • Pineda JC, Galarraga E, Bargas J, Cristancho M, Aceves J (1992) Charybdotoxin and apamin sensitivity of the calcium-dependent repolarization and the afterhyperpolarization in neostriatal neurons. J Neurophysiol 68:287–294

    CAS  PubMed  Google Scholar 

  • Powers AS, Reiner A (1980) A stereotaxic atlas of the forebrain and midbrain of the pattern painted turtle (Chrysemys picta picta). J Hirnforsch 21:125–159

    CAS  PubMed  Google Scholar 

  • Ramanathan S, Tkatch T, Atherton JF, Wilson CJ, Bevan MD (2008) D2-like dopamine receptors modulate SKCa channel function in subthalamic nucleus neurons through inhibition of 2 channels. J Neurophysiol 99:442–459

    Article  CAS  PubMed  Google Scholar 

  • Redgrave P, Presccott T, Gurney K (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89:1009–1023

    Article  CAS  PubMed  Google Scholar 

  • Reiner A (1987) The distribution of proenkephali-derived peptides in the central nervous system of turtles. J Comp Neurol 259:65–91

    Article  CAS  PubMed  Google Scholar 

  • Reiner A, Brauth SE, Kitt CA, Karten HJ (1980) Basal ganglionic pathways to the tectum: studies in reptiles. J Comp Neurol 193:565–589

    Article  CAS  PubMed  Google Scholar 

  • Reiner A, Brauth SE, Karten HJ (1984) Evolution of the amniote basal ganglia. TINS 7:320–325

    Google Scholar 

  • Reiner A, Medina L, Veenman CL (1998) Structural and functional evolution of the basal ganglia in vertebrates. Brain Res Rev 28:235–285

    Article  CAS  PubMed  Google Scholar 

  • Reyes A, Galarraga E, Flores-Hernández J, Tapia D, Bargas J (1998) Passive properties of neostriatal neurons during potassium conductance blockade. Exp Brain Res 120:70–84

    Article  CAS  PubMed  Google Scholar 

  • Richfield EK, Young AB, Penney JB (1987) Comparative distribution of dopamine D1 and D2 receptors in the basal ganglia of turtles, pigeons, rats, cats, and monkeys. J Comp Neurol 262:446–463

    Article  CAS  PubMed  Google Scholar 

  • Rieke GL (1981) Movement disorders and lesions of pigeon brainstem analogues of basal ganglia. Physiol Behav 26:379–384

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Mejorada E, Sánchez-Mondragon G, Pineda JC, González M, Barral J (2009) N-type of calcium channels mediates a GABAB presynaptic modulation of the corticostriatal synapses in turtle’s paleostriatum augmentatum. Synapse 63:855–862

    Article  PubMed  Google Scholar 

  • Smeets W (1994) Catecholamine system in the CNS of reptiles: structure and functional correlations. In: Smeets W, Reiner A (eds) Phylogeny and development of cathecholamine systems in the CNS of vertebrates. Cambridge University Press, Cambridge, pp 103–133

    Google Scholar 

  • Smeets W, Gonzalez A (2000) Catecholamine systems in the brain of vertebrates: new perspectives through a comparative approach. Brain Res Rev 33:308–379

    Article  CAS  PubMed  Google Scholar 

  • Smeets W, Jonker AJ, Hoogland PV (1987) The distribution of dopamine in the forebrain and midbrain of a turtle, Pseudemys scripta elegans, reinvestigated using antibodies against dopamine. Brain Behav Evol 30:121–142

    Article  CAS  PubMed  Google Scholar 

  • Smeets W, Marín O, González A (2000) Evolution of the basal ganglia: new perspectives through a comparative approach. J Anat 196:501–517

    Article  CAS  PubMed  Google Scholar 

  • Smeets W, Lopez JM, Gonzalez A (2003) Immunohistochemical localization of DARPP-32 in the brain of the turtle, Pseudemys scripta elegans: further assessment of its relationship with dopaminergic systems in reptiles. J Chem Neuroanat 25:83–95

    Article  CAS  PubMed  Google Scholar 

  • West AR, Grace AA (2002) Opposite influences of endogenous dopamine D1 and D2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 22:294–304

    CAS  PubMed  Google Scholar 

  • Wilson CJ (2004) The Basal ganglia. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford University Press, NY, pp 361–414

    Chapter  Google Scholar 

  • Yang CR, Seamans JK (1996) Dopamine D1 receptor actions in layers V–VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J Neurosci 16:1922–1935

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Beatriz Rubio Morales and Felipe Correa Sanchez from the Herpetology Lab of FES-Iztacala-UNAM for animal care. We also thank JA Laville for technical support and advice. This study was supported by: DGAPA Grants (IN201507 to EG, IN201607 to J Bargas, IN204407 to J Barral), PAPCA-2009-2010-FES Iztacala grant (to J Barral), and CONACyT grant (49484 to J Bargas, 81518 to J Barral).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jaime Barral.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barral, J., Galarraga, E., Tapia, D. et al. Dopaminergic Modulation of Spiny Neurons in the Turtle Striatum. Cell Mol Neurobiol 30, 743–750 (2010). https://doi.org/10.1007/s10571-010-9499-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10571-010-9499-7

Keywords

Navigation