Abstract
A mechanism for the involvement of the basal ganglia in the processing of visual information, based on dopamine-dependent modulation of the efficiency of synaptic transmission in interconnected parallel associative and limbic cortex-basal ganglia-thalamus-cortex circuits, is proposed. Each circuit consists of a visual or prefrontal area of the cortex connected with the thalamic nucleus and the corresponding areas in different nuclei of the basal ganglia. The circulation of activity in these circuits is supported by the recurrent arrival of information in the thalamus and cortex. Dopamine released in response to a visual stimulus modulates the efficiencies of “strong” and “weak” corticostriatal inputs in different directions, and the subsequent reorganization of activity in the circuit leads to disinhibition (inhibition) of the activity of those cortical neurons which are “strongly” (“weakly”) excited by the visual stimulus simultaneously with dopaminergic cells. The pattern in each cortical area is the neuronal reflection of the properties of the visual stimulus processed by this area. Excitation of dopaminergic cells by the visual stimulus via the superior colliculi requires parallel activation of the disinhibitory input to the superior colliculi via the thalamus and the “direct” pathway” in the basal ganglia. The prefrontal cortex, excited by the visual stimulus via the mediodorsal nucleus of the thalamus, mediates the descending influence on the activity of dopaminergic cells, simultaneously controlling dopamine release in different areas of the striatum and thus facilitating the mutual selection of neural reflections of the individual properties of the visual stimulus and their binding into an integral image.
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L. F. Burchinskaya, V. S. Zelenskaya, V. A. Cherkes, and B. P. Kolomiets, “Pathways for the transmission of visual and auditory information to the caudate nucleus in the cat,” Neirofiziologiya, 19, No. 4, 512–520 (1987).
N. V. Veber, S. Sh. Rapoport, I. G. Sil’kis, and S. S. Sokolov, “Longterm posttetanic changes in the spike responses of visual cortex neurons in the cat,” Zh. Vyssh. Nerv. Deyat., 38, No. 5, 963–965 (1988).
V. D. Glezer, N. V. Prazdnikova, L. I. Leushina, A. A. Nevskaya, and M. B. Pavlovskaya, Recognition of Visual Objects. Visual Physiology [in Russian], Nauka, Moscow (1992), pp. 466–527.
A. M. Ivanitskii, “A major natural mystery: how brain function generates subjective experiences,” Psikhol. Zh., 20, No. 3, 93–104 (1999).
B. P. Kolomiets, “Electrophysiological studies of the effects of stimulating the pulvinar on caudate nucleus neurons responding to visual stimulation,” Neirofiziologiya, 23, No. 5, 520–529 (1991).
A. M. Mass and A. Ya. Supin, Functional Organization of the Superior Colliculi in Mammals [in Russian], Nauka, Moscow (1985).
I. N. Pigarev, “Extrastriate visual zones in the cerebral cortex,” in: Visual Physiology [in Russian], Nauka, Moscow (1992), pp. 345–400.
N. S. Podvigin, “Processing of signals in the intermediate and midbrain,” in Visual Physiology [in Russian], Nauka, Moscow (1992), pp. 162–242.
N. V. Prazdnikova, V. D. Glezer, and V. F. Danilova, “Two types of generalization in the evolution of the visual brain,” Zh. Évolyuts. Biokhim. Fiziol., 21, No. 5, 435–442 (1985).
I. G. Sil’kis, “The role of the basal ganglia in generating dreams in paradoxical sleep (a hypothetical mechanism),” Zh. Vyssh. Nerv. Deyat., 56, No. 1, 5–21 (2006).
I. G. Sil’kis, “The role of the basal ganglia in generating visual hallucinations (a hypothetical mechanism),” Zh. Vyssh. Nerv. Deyat., 55, No. 5, 592–607 (2005).
I. G. Sil’kis, “A possible mechanism for the role of dopaminergic cells and cholinergic interneurons in the striatum in the conditioned reflex selection of motor activity,” Zh. Vyssh. Nerv. Deyat., 54, No. 6, 734–749 (2004).
I. G. Sil’kis, “Possible mechanisms of the effects of endogenous neuromodulators on the mutually dependent activity of neurons in the various nuclei of the basal ganglia,” Ros. Fiziol. Zh., 90, No. 3, 282–293 (2004).
I. G. Sil’kis, “Effects of neuromodulators on synaptic plasticity in dopaminergic structures of the midbrain (a hypothetical mechanism),” Zh. Vyssh. Nerv. Deyat., 53, No. 4, 464–479 (2003).
I. G. Sil’kis, “Involvement of dopamine in enhancing cortical signals activating NMDA receptors in the striatum (a hypothetical mechanism),” Ros. Fiziol. Zh., 87, No. 12, 1569–1578 (2001).
I. G. Sil’kis and S. Sh. Rapoport, “Comparative analysis of the latent periods of responses of close-lying neurons in visual cortex microzones,” Zh. Vyssh. Nerv. Deyat., 33, No. 5, 877–884 (1983).
V. A. Cherkes and V. S. Zelenskaya, “Responses of caudate nucleus neurons to various visual stimuli in actively conscious rats,” Neirofiziologiya, 15, No. 4, 370–376 (1983).
I. A. Shevelev, “The functional importance of the primary responses of the subcortical visual centers,” Zh. Vyssh. Nerv. Deyat., 21, No. 3, 569–576 (1971).
V. T. Shuvaev and N. F. Suvorov, The Basal Ganglia and Behavior [in Russian], Nauka, St. Petersburg (2001).
H. D. Abraham and F. H. Duffy, “EEG coherence in post-LSD visual hallucinations,” Psychiatry Res., 107, No. 3, 151–163 (2001).
A. Antal, S. Keri, T. Kincses, J. Kalman, G. Dibo, G. Benedek, Z. Janka, and L. Vecsei, “Corticostriatal circuitry mediates fast-track visual categorization,” Cogn. Brain Res., 13, No. 1, 53–59 (2002).
T. Aosaki, M. Kimura, and A. M. Graybiel, “Temporal and spatial characteristics of tonically active neurons of the primate’s striatum,” J. Neurophysiol., 73, No. 3, 1234–1252 (1995).
H. E. Atallah, M. J. Frank, and R. C. O’Reilly, “Hippocampus, cortex, and basal ganglia: insights from computational models of complementary learning systems,” Neurobiol. Learn. Mem., 82, No. 3, 253–267 (2004).
B. J. Baars, “The conscious access hypothesis: origins and recent evidence,” Trends Cogn. Sci., 6, No. 1, 47–52 (2002).
E. H. Bertram and D. X. Zhang, “Thalamic excitation of hippocampal CA1_neurons: a comparison with the effects of CA3_stimulation,” Neuroscience, 92, No. 1, 15–26 (1999).
I. Bodis-Wollner, “Neuropsychological and perceptual defects in Parkinson’s disease,” Parkinsonism Relat. Disord., 9, Supplement 2, S83–S89 (2003).
C. E. Boudreau and D. Ferster, “Short-term depression in thalamocortical synapses of cat primary visual cortex,” J. Neurosci., 25, No. 31, 7179–7190 (2005).
V. J. Brown, R. Desimone, and M. Mishkin, “Responses of cells in the tail of the caudate nucleus during visual discrimination learning,” J. Neurophysiol., 74, No. 3, 1083–1094 (1995).
L. L. Brown, J. S. Schneider, and T. I. Lidsky, “Sensory and cognitive functions of the basal ganglia,” Curr. Opin. Neurobiol., 7, No. 2, 157–163 (1997).
T. Buttner, W. Kuhn, T. Patzold, and H. Przuntek, “L-Dopa improves colour vision in Parkinson’s disease,” J. Neural Transm. Park. Dis. Dement. Sect., 7, No. 1, 13–29 (1994).
G. G. Celesia, M. G. Brigell, and M. S. Vaphiades, “Hemianopic anosognosia,” Neurology, 49, No. 1, 88–97 (1997).
E. Comoli, V. Coizet, J. Boyes, J. P. Bolam, N. S. Canteras, R. H. Quirk, P. G. Overton, and P. Redgrave, “A direct projection from superior colliculus to substantia nigra for detecting salient visual events,” Nat. Neurosci., 6, No. 9, 974–980 (2003).
F. Crick and C. Koch, “Are we aware of neuronal activity in primary visual cortex?” Nature, 375, No. 625, 121–123 (1995).
J. M. Deniau, A. Menetrey, and S. Charpier, “The lamellar organization of the rat substantia nigra pars reticulata: segregated patterns of striatal afferents and relationship to the topography of corticostriatal projections,” Neuroscience, 73, No. 3, 761–781 (1996).
E. Dommett, V. Coizet, C. D. Blaha, J. Martindale, V. Lefebvre, N. Walton, J. E. Mayhew, P. G. Overton, and P. Redgrave, “How visual stimuli activate dopaminergic neurons at short latency,” Science, 307, No. 5714, 1476–1479 (2005).
N. N. Doron and J. E. Ledoux, “Organization of projections to the lateral amygdala from auditory and visual areas of the thalamus in the rat,” J. Comp. Neurol., 412, No. 3, 383–409 (1999).
M. C. Gaillard and F. X. Borruat, “Persisting visual hallucinations and illusions in previously drug-addicted patients,” Klin. Monatsbl. Augenheilkd., 220, No. 3, 176–178 (2003).
J. M. Gimenez-Amaya, S. de las Heras, E. Erro, E. Mengual, and J. L. Lanciego, “Considerations on the thalamostriatal system with some functional implications,” Histol. Histopathol., 15, No. 4, 1285–1292 (2000).
H. J. Groenewegen, Y. Galis-de Graar, and W. J. Smeets, “Integration and segregation of limbic cortico-striatal loops at the thalamic level: an experimental tracing study in rats,” J. Chem. Neuroanat., 16, No. 3, 167–185 (1999).
K. Gurney, T. J. Prescott, and P. Redgrave, “A computational model of action selection in the basal ganglia. II. Analysis and simulation of behaviour,” Biol. Cybern., 84, No. 6, 411–423 (2001).
S. N. Haber, “The primate basal ganglia: parallel and integrative networks,” J. Chem. Neuroanat., 26, No. 4, 317–330 (2003).
J. K. Harting, B. V. Updyke, and D. P. Lieshout, “Striatal projections from the cat visual thalamus,” Eur. J. Neurosci., 14, No. 5, 893–896 (2001).
A. J. Heynen and M. F. Bear, “Long-term potentiation of thalamocortical transmission in the adult visual cortex in vivo,” J. Neurosci., 21, No. 24, 9801–9813 (2001).
O. Hikosaka, Y. Takikawa, and R. Kawagoe, “Role of the basal ganglia in the control of purposive saccadic eye movements,” Physiol. Rev., 80, No. 3, 954–978 (2000).
J. C. Horvitz, “Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events,” Neuroscience, 96, No. 3, 651–656 (2000).
M. Inoue, Y. Katsumi, T. Hayashi, T. Mukai, K. Ishizu, K. Hashikawa, H. Saji, and J. Fukuyama, “Sensory stimulation accelerates dopamine release in the basal ganglia,” Brain Res., 1026, No. 2, 179–184 (2004).
J. P. Joseph and D. Boussaoud, “Role of the cat substantia nigra pars reticulata in eye and head movements. I. Neural activity,” Exptl. Brain Res., 57, No. 2, 286–296 (1985).
B. Kolomiets, “A possible visual pathway to the cat caudate nucleus involving the pulvinar,” Exptl. Brain Res., 97, No. 2, 317–324 (1993).
R. Lape and J. A. Dani, “Complex response to afferent excitatory bursts by nucleus accumbens medium spiny projection neurons,” J. Neurophysiol., 92, No. 3, 1276–1284 (2004).
M.S. Lees, J. O. Rinne, and C. D. Marsden, “The pedunculopontine nucleus: its role in the genesis of movement disorders,” Yonsei Med. J., 41, No. 2, 167–184 (2000).
J. H. Maunsell and J. R. Gibson, “Visual response latencies in striate cortex of the macaque monkey,” J. Neurophysiol., 68, No. 4, 1332–1344 (1992).
N. R. McFarland and S. N. Haber, “Thalamic relay nuclei of the basal ganglia form both reciprocal and nonreciprocal cortical connections, linking multiple frontal cortical areas,” J. Neurosci., 22, No. 18, 8117–8132 (2002).
A. Mele, M. Avena, P. Roullet, R. de Leonibus, S. Mandillo, F. Sargolini, R. Coccurello, and A. Oliveiro, “Nucleus accumbens dopamine receptors in the consolidation of spatial memory,” Behav. Pharmacol., 15, No. 5–6, 423–431 (2004).
M. M. Mesulam, “Dopamine agonists reorient visual exploration away from the neglected hemispace,” Neurology, 51, No. 5, 1395–1398 (1998).
F. A. Middleton and P. L. Strick, “Basal-ganglia ’projections’ to the prefrontal cortex of the primate,” Cereb. Cortex, 12, No. 9, 926–935 (2002).
F. A. Middleton and P. L. Strick, “Basal ganglia output and cognition: evidence from anatomical, behavioral, and clinical studies,” Brain Cogn., 42, No. 2, 183–200 (2000).
F. A. Middleton and P. L. Strick, “The temporal lobe is a target of output from the basal ganglia,” Proc. Natl. Acad. Sci. USA, 93, No. 16, 8683–8687 (1996).
H. Mollion, J. Ventre-Dominey, P. F. Dominey, and E. Broussolle, “Dissociable effects of dopaminergic therapy on spatial versus nonspatial working memory in Parkinson’s disease,” Neuropsychologia, 41, No. 11, 1442–1451 (2003).
M. F. Montaron, J. M. Deniau, A. Menetrey, J. Glowinski, and A. M. Thierry, “Prefrontal cortex inputs of the nucleus accumbensnigro-thalamic circuit,” Neuroscience, 71, No. 2, 371–382 (1996).
M. H. Munk, L. G. Nowak, P. Girard, N. Chounlamountri, and J. Bullier, “Visual latencies in cytochrome oxidase bands of macaque area V2,” Proc. Natl. Acad. Sci. USA, 92, No. 4, 988–992 (1995).
A. Nagy, G. Eordegh, M. Norita, and G. Benedek, “Visual receptive field properties of excitatory neurons in the substantia nigra,” Neuroscience, 130, No. 2, 513–518 (2005).
A. Nagy, G. Eordegh, M. Norita, and G. Benedek, “Visual receptive field properties of neurons in the caudate nucleus,” Eur. J. Neurosci., 18, No. 2, 449–452 (2003).
T. Niida, B. E. Stain, and J. G. McHaffie, “Response properties of corticotectal and corticostriatal neurons in the posterior lateral suprasylvian cortex of the cat,” J. Neurosci., 17, No. 21, 8550–8565 (1997).
A. Parent and L. N. Hazrati, “Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop,” Brain Res. Rev., 20, No. 1, 91–127 (1995).
A. Parent and L. N. Hazrati, “Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry,” Brain Res. Rev., 20, No. 1, 128–154 (1995).
M. Just Price, R. G. Feldman, D. Adelberg, and H. Kayne, “Abnormalities in color vision and contrast sensitivity in Parkinson’s disease,” Neurology, 42, No. 4, 887–890 (1992).
A. Priori, C. Cinnante, S. Genitrini, A. Pesenti, G. Tortora, C. Bencini, M. V. Barelli, V. Buonamici, F. Carella, F. Girotti, P. Soliveri, F. Magrini, A. Morganti, A. Albanese, S. Broggi, G. Scarlato, and S. Barbieri, “Non-motor effects of deep brain stimulation of the subthalamic nucleus in Parkinson’s disease: preliminary physiological results,” Neurol. Sci., 22, No. 1, 85–86 (2001).
I. Rektor, M. Bares, M. Brazdil, P. Kanovsky, I. Rektorova, D. Sochurkova, D. Kubova, R. Kuba, and P. Daniel, “Cognitive-and movement-related potentials recorded in the human basal ganglia,” Mov. Disord., 20, No. 5, 562–568 (2005).
J. Ribas, J. M. Delgado-Garcia, A. Lopez-Beltran, and D. Mir, “A morphological and electrophysiological study of nigrotectal pathway in the rat,” Rev. Esp. Fisiol., 37, No. 1, 45–52 (1981).
R. L. Rodnitzky, “Visual dysfunction in Parkinson’s disease,” Clin. Neurosci., 5, No. 2, 102–106 (1998).
A. F. Sadikot, A. Arent, Y. Smith, and J. P. Bolam, “Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity,” J. Comp. Neurol., 320, No. 2, 228–242 (1992).
M. T. Schmolesky, Y. Wang, D. P. Hanes, K. G. Thompson, S. Leutgeb, J. D. Schall, and A. G. Leventhal, “Signal timing across the macaque visual system,” J. Neurophysiol., 79, No. 6, 3272–3278 (1998).
J. S. Schneider, “Basal ganglia role in behavior: importance of sensory gating and its relevance to psychiatry,” Biol. Psychiatry, 19, No. 12, 1693–1710 (1984).
U. Schroeder, A. Kueler, A. Hennenlotter, B. Haslinger, V. M. Tronnier, M. Krause, R. Pfister, R. Sprengelmayer, K. W. Lange, and A. O. Ceballos-Baumann, “Facial expression recognition and subthalamic nucleus stimulation,” J. Neurol. Neurosurg. Psychiatry, 75, No. 4, 648–650 (2004).
W. Schultz and R. Romo, “Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions,” J. Neurophysiol., 63, No. 3, 607–624 (1990).
H. Sherk and K. A. Mulligan, “Retinotopic order is surprisingly good within cell columns in the cat’s lateral suprasylvian cortex,” Exptl. Brain Res., 91, No. 1, 46–60 (1992).
S. M. Sherman and R. W. Guillery, “The role of the thalamus in the flow of information to the cortex,” Phil. Trans. Roy. Soc. Lond., B. Biological Sciences, 357, No. 428, 1695–1708 (2002).
I. A. Shevelev, N. A. Lazareva, G. A. Sharaev, R. V. Novikova, and A. S. Tikhomirov, “Interrelation of tuning characteristics to bar, cross and corner in striate neurons,” Neuroscience, 88, No. 1, 17–25 (1999).
M. Sidibe and Y. Smith, “Differential synaptic innervation of striatofugal neurones projecting to the internal or external segments of the globus pallidus by thalamic afferents in the squirrel monkey,” J. Comp. Neurol., 365, No. 3, 445–465 (1996).
H. Tokuno, M. Takada, Y. Kondo, and N. Mizuno, “Laminar organization of the substantia nigra pars reticulata in the macaque monkey, with special reference to the caudato-nigro-tectal link,” Exptl. Brain Res., 92, No. 3, 545–548 (1993).
Z. Y. Tong, P. G. Overton, and D. Clark, “Stimulation of the prefrontal cortex in the rat induces patterns of activity in midbrain dopaminergic neurons which resemble natural burst events,” Synapse, 22, No. 3, 195–208 (1996).
F. J. Varedas, F. J. Vico, and J. M. Alonso, “Factors determining the precision of the correlated firing generated by a monosynaptic connection in the cat visual pathway,” J. Physiol., 567, No. 3, 1057–1078 (2005).
L. Wang, Y. Kuroiwa, M. Li, J. Wag, and T. Kamitani, “Do Pl and Nl evoked by the ERP task reflect primary visual processing in Parkinson’s disease?” Doc. Ophthalmol., 102, No. 2, 83–93 (2001).
J. Yelnik, “Functional anatomy of the basal ganglia,” Mov. Disord., 17,Supplement 3, S15–S21 (2002).
M. T. Zagami, M. E. Montalbano, M. Sabatino, and V. La Grutta, “Effect of acetylcholine and dopamine iontophoretically applied on the sensory responsive caudate unit,” Arch. Int. Physiol. Biochim., 94, No. 5, 305–316 (1986).
S. Zeki, “Localization and globalization in conscious vision,” Ann. Rev. Neurosci., 24, 57–86 (2001).
S. Zeki and A. Bartels, “The autonomy of the visual systems and the modularity of conscious vision,” Phil. Trans. Roy. Soc. Lond., B. Biological Sciences, 353, No. 1377, 1911–1914 (1998).
C. F. Zink, G. Pagnoni, M. E. Martin, M. Dhamala, and G. S. Berns, “Human striatal response to salient nonrewarding stimuli,” J. Neurosci., 23, No. 22, 8092–8097 (2003).
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Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 56, No. 6, pp. 742–756, November–December, 2006.
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Sil’kis, I.G. The contribution of synaptic plasticity in the basal ganglia to the processing of visual information. Neurosci Behav Physiol 37, 779–790 (2007). https://doi.org/10.1007/s11055-007-0082-8
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DOI: https://doi.org/10.1007/s11055-007-0082-8