Abstract
Studies on 60 Sprague-Dawley rats were performed to compare systemic and intrastriate administration of the selective D1 dopamine receptor blocker SCH23390 on the acquisition of a discriminant conditioned active avoidance reflex (CAAR) in a T maze and on behavior in an open field test. Systemic treatment at a dose of 0.025 mg/kg produced several-fold reductions in the proportion of correct performances of the discriminant CAAR and motor activity in the open field test. At the same time, bilateral microinjection of SCH23390 into the rat neostriatum at doses of 0.004–1.0 µg did not induce any deterioration in learning of the discriminant CAAR as compared with intact controls, though there was a sharp inhibition of motor activity in the open field test. Bilateral microinjections of the D2 dopamine receptor blocker raclopride into the rat neostriatum at a dose of 0.004 µg produced a marked and long-lasting degradation of learning of the discriminant CAAR. These data lead to the following conclusions: 1) the differences in the effects of systemic and intrastriate administration of SCH23390 appear to be associated with the fact that the behavioral changes seen after systemic administration may be mediated mainly by structures differing from neostriatal D1 receptors, and 2) the D1-mediated effects of the nigrostriatal dopaminergic system on the neostriatum are complex, with activation of motor activity (projection spiny neurons of the direct pathway) and weak modulation of the learning process (large aspiny cholinergic interneurons). Modulation of the learning process evidently occurs via neostriatal D2 dopaminergic receptors.
Similar content being viewed by others
References
Yu. S. Borodkin and I. D. Shabanov, Neurophysiological Mechanisms of Memory Trace Extraction [in Russian], Nauka, Leningrad (1986).
N. I. Dubrovina and L. V. Loskutova, Dopaminergic Mechanisms of Memory and Attention [in Russian], Siberian Branch, Russian Academy of Medical Sciences, Novosibirsk (2003).
V. N. Maiorov and A. G. Frolov, “Effects of systemic administration of selective antagonists of dopamine D1 and D2/3 receptors on food-related and motivational (escape reaction) conditioned paw-placing reflexes in cats,” Zh. Vyssh. Nerv. Deyat., 54, No. 4, 489–494 (2004).
N. F. Suvorov, N. B. Saul’skaya, and O. G. Chivileva, “The striatonigral level of the neurochemical organization of conditioned avoidance reflexes of different levels of complexity.” Zh. Vyssh. Nerv. Deyat., 32, No. 2, 276–283 (1982).
K. B. Shapovalova, E. V. Pominova, and T. A. Dyubkacheva, “Characteristics of the effects of the cholinergic system of the rat neostriatum on learning active avoidance in normal conditions and after lesioning of the inatralaminar nuclei of the thalamus,” Ros. Fiziol. Zh. im. I. M. Sechenova, 82, No. 1, 1–12 (1996).
K. B. Shapovalova, Yu. V. Kamkina, and D. A. Mysovskii, “Effects of microinjections of the selective muscarinic M1 receptor blocker pirenzipine into the neostriatum on motor behavior in rats,” Ros. Fiziol. Zh. im. I. M. Sechenova, 90, No. 2, 129–136 (2004).
A. F. Yakimovskii and I. V. Karpova, “Effects of chronic activation and blockade of the dopaminergic and enkephalinergic systems of the neostriatum on conditioned reflex behavior and dopamine metabolism in the nigrostriatal system in rats,” Zh. Vyssh. Nerv. Deyat., 42, No. 5, 930–936 (1992).
W. Adriani, F. Sargolini, and R. Coccurello, “Role of dopaminergic system in reactivity to spatial and non-spatial changes in mice,” Psychopharmacology, 150, No. 1, 67–76 (2000).
T. Aosaki, H. Tsubokawa, A. Ishida, K. Watanabe, A. Graybiel, and M. Kimura, “Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning,” J. Neurosci., 14, No. 6, 3969–3984 (1994).
A. E. Baldwin, K. Sadeghian, and A. E. Kelly, “Appetitive instrumental learning requires coincident activation of NMDA and dopamine Dl receptors within the medial prefrontal cortex,” J. Neurosci., 22, No. 3, 1053–1071 (2002).
R. J. Beninger, “The role of dopamine in locomotor activity and learning,” Brain Res. Rev., 6, 173–196 (1983).
R. J. Beninger, “Dissociating the effects of altered dopaminergic function on performance and learning,” Brain Res. Bull., 23, 365–371 (1989).
J. R. Blackburn and A. G. Phillips, “Blockade of acquisition of one-way conditioned avoidance responding by haloperidol and metoclopramide but not by thioridazine and clozapine: implications for screening new antipsychotic drugs,” Psychopharmacol. (Berlin), 98, 453–459 (1989).
C. Contant, D. Umbriaco, S. Garcia, K. Watkins, and J. Descaries, “Ultrastructural organization of the acetylcholine innervation in adult rat neostriatum,” Neurosci., 13, No. 4, 937–947 (1996).
J. F. Flood, G. E. Smith, E. L. Bennett, et al., “Neurochemical and behavioral effects of catecholamine and protein synthesis inhibitions in mice,” Pharmacol. Biochem. Behav., 24, No. 3, 631–645 (1986).
C. Gerfen, “The neostriatal mosaic organization in the basal ganglia,” Ann. Rev. Neurosci., 15, No. 2, 285–329 (1992).
F. A. Guarrachi, R. J. Flohardt, W. A. Falls, and B. S. Kapp, “The effects of intraamygdaloid infusions of a D2 dopamine receptor antagonists on Pavlovian fear conditioning,” Behav. Neurosci., 14, No. 3, 647–651 (2000).
W. Heuber, “Involvement of basal ganglia transmitter systems,” Progr. Neurobiol., 56, No. 3, 507–540 (1998).
E. Ince, B. J. Cillias, and A. Levey, “Differential organization of Dl and D2 dopamine and m4 muscarinic acetylcholine receptors protein in identified striatonigral neurons,” Synapse, 27, No. 3, 357–362 (1997).
T. Inone, Y. Maki, I. Muraki, and T. Koyama, “Effect of the dopamine D (1/5) antagonist SCH 23390 on the acquisition of conditioned fear,” Pharmacol. Biochem. Behav., 66, No. 3, 573–578 (2000).
H. Kamei, T. Kameyama, and T. Nabeshima, “Activation of both dopamine Dl and D2 receptors necessary for amelioration of conditioned fear stress,” Eur. J. Pharmacol., 273, No. 3, 229–233 (1995).
M. Kimura, M. Kato, H. Shimazaki, K. Watanabe, and N. Matsumoto, “Neural information transferred from the putamen to the globus pallidus during learned movement in the monkey,” J. Neurophysiol., 76, No. 6, 3771 (1996).
N. Koshikawa, “Role of the nucleus accumbens and the striatum in the production of turning behavior in intact rats,” Rev. Neurosci., 5, No. 4, 331–346 (1994).
Y. Kubota, S. Inagaki, S. Shimada, S. Kito, F. Eckenstein, and M. Tayama, “Neostriatal cholinergic neurons receive direct synaptic inputs from dopaminergic neurons,” Brain Res., 413, No. 2, 179–184 (1987).
M. J. Packard and N. M. White, “Memory facilitation produced by dopamine receptor agonists: role of receptor subtype and mnemonic requirement,” Pharmacol. Biochem. Behav., 33, No. 4, 511–518 (1986).
A. Parent and B. Lavoie, “Dopaminergic innervation of the basal ganglia in normal and Parkinsonian monkeys,” in: Current Concepts in Parkinson’s Disease Research, J. S. Schneider and M. Gupta (eds.), Hans Teuber, Toronto (1993).
M. A. Pezze, C. A. Heidbreder, J. Feldon, and C. A. Murphy, “Selective responding of nucleus accumbens core and shell dopamine to aversively conditioned contextual and discrete stimuli,” Neurosci., 108, No. 1, 91–102 (2001).
J. N. Picada, N. Schroder, I. Izquierdo, et al., “Differential neurobehavioral deficits induced by apomorphine and its oxidation product, 8-oxo-apomorphine in rats,” Eur. J. Pharmacol., 443, No. 1–3, 105–111 (2002).
R. Ranandi and R. J. Beninger, “The effects of systemic and intracerebral injections of D-l and D-2 agonists on brain stimulation reward,” Brain Res., 651, No. 1–2, 283–292 (1992).
W. Schultz, “Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey,” J. Neurophysiol., 56, No. 6, 1439–1461 (1986).
J. L. Seamans, S. B. Floresco, and A. G. Phillips, “Dl receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory and executive functions in the rat,” J. Neurosci., 18, No. 4, 1613–1621 (1998).
R. H. Silva, S. R. Kameda, R. C. Carvalho, et al., “Effects of amphetamine on the plus-maze discriminative avoidance task in mice,” Psychopharmacol., 160, No. 1, 9–18 (2002).
B. J. Strupp, M. Bunney, D. Livitsky, and M. Kesler, “Time-dependent effects of post-trial amphetamine treatment in rats: evidence for enhanced storage of representational memory,” Behav. Neurol. Biol., 56, No. 1, 67–76 (1991).
M. Tzschentke, “Pharmacology and behavioral pharmacology of the mesocortical dopamine system,” Progr. Neurobiol., 63, No. 3, 241–320 (2001).
L. O. Wang and J. F. McGinty, “Muscarinic receptors regulate striatal neuropeptide gene expression on normal and amphetamine treated rats,” Neurosci., 75, No. 1, 43–50 (1996).
K. Watanabe and M. Kimura, “Dopamine receptor — mediated mechanisms involved in the expression of learned activity of primate striatal neurons,” J. Neurophysiol., 79, No. 6, 2568–2580 (1998).
N. M. White, M. G. Packard, and J. Seamans, “Memory enhancement by post-training peripheral administration of low doses of dopamine agonists: possible autoreceptor effect,” Behav. Neurol. Biol., 59, No. 2, 230–241 (1993).
R. A. Wise, “Neuroleptics and operant behavior: the anhedonia hypothesis,” Behav. Brain Sci., 5, No. 1, 39–87 (1982).
S. Yasumoto, E. Tanaka, G. Hattori, H. Maeda, and H. Higashi, “Direct and indirect actions of dopamine on the membrane potential in medium spiny neurons of the mouse neostriatum,” J. Neurophysiol., 82, 1234–1243 (2002).
Author information
Authors and Affiliations
Additional information
__________
Translated from Rossiiskii Fiziologicheskii Zhurnal imeni I. M. Sechenova, Vol. 92, No. 10, pp. 1173–1186, October, 2006.
Rights and permissions
About this article
Cite this article
Shapovalova, K.B., Kamkina, Y.V. Motor and cognitive functions of the neostriatum during bilateral blockade of its dopamine receptors. Neurosci Behav Physi 38, 71–79 (2008). https://doi.org/10.1007/s11055-008-0010-6
Received:
Issue Date:
DOI: https://doi.org/10.1007/s11055-008-0010-6