Effects of local connectivity on striatal function: Simulation and analysis of a model

Neuronal population activity was investigated by computer simulation of a network model based on the neostriatum. Three network topologies were studied, based on different assumptions about the synaptic connectivity among medium spiny neurons. In all networks neurons were interconnected by inhibitory synapses. The connectivity was either symmetric, in which case all connections between cells were reciprocal and equal in strength; or asymmetric. Simulations showed that networks with symmetric connectivity receiving randomly distributed afferent excitation produced stationary spatial activity patterns. In contrast, asymmetric connectivity in homogeneous networks produced slow travelling‐wave activity across the network. We suggest that the shape of the medium spiny neurons is an important determinant of synaptic connectivity and that changes in the shape of these neurons caused by Huntington's disease would result in asymmetric connectivity. Slow travelling‐wave activity produced by asymmetric connectivity in the neostriatum could explain some aspects of the choreic movement and some electromyographic features seen in Huntington's patients. © 1995 Wiley‐Liss, Inc.

[1]  S. A. Wilson,et al.  PROGRESSIVE LENTICULAR DEGENERATION: A FAMILIAL NERVOUS DISEASE ASSOCIATED WITH CIRRHOSIS OF THE LIVER , 1912 .

[2]  T. J. Putnam,et al.  ACTION POTENTIALS OF MUSCLES IN ATHETOSIS AND SYDENHAM'S CHOREA , 1940 .

[3]  G LUNDIN,et al.  SOLUBILITY OF ACETYLENE IN LUNG TISSUE AS AN ERROR IN CARDIAC OUTPUT DETERMINATION WITH THE ACETYLENE METHOD. , 1963, Acta physiologica Scandinavica.

[4]  C. Rocha-Miranda Single unit analysis of cortex-caudate connections. , 1965, Electroencephalography and clinical neurophysiology.

[5]  T. Powell,et al.  The structure of the caudate nucleus of the cat: light and electron microscopy. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  M. Delong,et al.  Putamen: Activity of Single Units during Slow and Rapid Arm Movements , 1973, Science.

[7]  N. A. Buchwald,et al.  Caudate intracellular response to thalamic and cortical inputs. , 1973, Experimental neurology.

[8]  P. Copack,et al.  Intrinsic connections of caudate neurons. Locally evoked intracellular responses. , 1973, Experimental neurology.

[9]  S. L. Liles Single-unit responses of caudate neurons to stimulation of frontal cortex, substantia nigra and entopeduncular nucleus in cats. , 1974, Journal of neurophysiology.

[10]  B. Cohen,et al.  Afferent modulation of unit activity in globus pallidus and caudate nucleus: changes induced by vestibular nucleus and pyramidal tract stimulation , 1975, Brain Research.

[11]  G. Bernardi,et al.  The action of picrotoxin and bicuculline on rat caudate neurons inhibited by GABA , 1976, Brain Research.

[12]  J. Coyle,et al.  Lesion of striatal neurons with kainic acid provides a model for Huntington's chorea , 1976, Nature.

[13]  P. Mcgeer,et al.  A glutamatergic corticostriatal path? , 1977, Brain Research.

[14]  R. Porter,et al.  Cells of origin and terminal distrubution of corticostriatal fibers arising in the sensory‐motor cortex of monkeys , 1977, The Journal of comparative neurology.

[15]  H. Mclennan,et al.  Mechanisms of excitation and inhibition in the nigrostriatal system , 1977, Brain Research.

[16]  T. Pasik,et al.  A golgi study of afferent fibers in the neostriatum of monkeys , 1978, Brain Research.

[17]  M. Sugimori,et al.  Response properties and electrical constants of caudate nucleus neurons in the cat. , 1978, Journal of neurophysiology.

[18]  Charles J. Wilson,et al.  Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: A study employing intracellular injection of horseradish peroxidase , 1980 .

[19]  Melburn R. Park,et al.  Recurrent inhibition in the rat neostriatum , 1980, Brain Research.

[20]  S. T. Kitai,et al.  Medium spiny neuron projection from the rat striatum: An intracellular horseradish peroxidase study , 1980, Brain Research.

[21]  C. Goetz,et al.  Levodopa and presymptomatic detection of Huntington's disease--eight-year follow-up. , 1980, The New England journal of medicine.

[22]  P. Somogyi,et al.  Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the golgi‐peroxidase transport‐degeneration procedure , 1981, The Journal of comparative neurology.

[23]  Charles J. Wilson,et al.  Spontaneous firing patterns of identified spiny neurons in the rat neostriatum , 1981, Brain Research.

[24]  J. W. Lighthall,et al.  Inhibition in slices of rat neostriatum , 1981, Brain Research.

[25]  Y. Katayama,et al.  Electrophysiological evidence favoring intracaudate axon collaterals of GABAergic caudate output neurons in the cat , 1981, Brain Research.

[26]  P. Goldman-Rakic Cytoarchitectonic heterogeneity of the primate neostriatum: Subdivision into island and matrix cellular compartments , 1982, The Journal of comparative neurology.

[27]  S. T. Kitai,et al.  Morphological and physiological properties of neostriatal neurons: An intracellular horseradish peroxidase study in the rat , 1982, Neuroscience.

[28]  D. A. Brown,et al.  M‐currents and other potassium currents in bullfrog sympathetic neurones , 1982, The Journal of physiology.

[29]  P. Groves A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement , 1983, Brain Research Reviews.

[30]  N. A. Buchwald,et al.  Intracellular studies of the convergence of sensory input on caudate neurons of cat , 1983, Brain Research.

[31]  J. W. Lighthall,et al.  A short duration GABAergic inhibition in identified neostriatal medium spiny neurons: In vitro slice study , 1983, Brain Research Bulletin.

[32]  T. Kita,et al.  Passive electrical membrane properties of rat neostriatal neurons in an in vitro slice preparation , 1984, Brain Research.

[33]  J. Rajkowski,et al.  Tonically discharging putamen neurons exhibit set-dependent responses. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[34]  A. Graybiel Correspondence between the Dopamine islands and striosomes of the mammalian striatum , 1984, Neuroscience.

[35]  G. Graveland,et al.  A Golgi study of the human neostriatum: Neurons and afferent fibers , 1985, The Journal of comparative neurology.

[36]  G. E. Alexander,et al.  Microstimulation of the primate neostriatum. I. Physiological properties of striatal microexcitable zones. , 1985, Journal of neurophysiology.

[37]  G. Graveland,et al.  Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. , 1985, Science.

[38]  R. Ferrante,et al.  Neuropathological Classification of Huntington's Disease , 1985, Journal of neuropathology and experimental neurology.

[39]  N. A. Buchwald,et al.  Neurons of origin of striatonigral axons in the cat: connectivity and Golgi markers of somatodendritic architecture , 1986, Brain Research.

[40]  I. Kanazawa,et al.  ‘Choreic’ movement induced by unilateral kainate lesion of the striatum and l-DOPA administration in monkey , 1986, Neuroscience Letters.

[41]  G. Porenta A computer model of neuronal pathways in the basal ganglia. , 1986, Computer methods and programs in biomedicine.

[42]  K. Chase,et al.  Glutamic acid decar☐ylase and enkephalin immunoreactive axon terminals in the rat neostriatum synapse with striatonigral neurons , 1986, Brain Research.

[43]  P. Calabresi,et al.  Intrinsic membrane properties of neostriatal neurons can account for their low level of spontaneous activity , 1987, Neuroscience.

[44]  K. Heilman,et al.  Response time in monkeys with unilateral neglect. , 1987, Archives of neurology.

[45]  C. Sikström,et al.  Population Studies in Northern Sweden , 1988 .

[46]  P. Thompson,et al.  The coexistence of bradykinesia and chorea in Huntington's disease and its implications for theories of basal ganglia control of movement. , 1988, Brain : a journal of neurology.

[47]  J. B. Martin,et al.  Clinical and neuropathologic assessment of severity in Huntington's disease , 1988, Neurology.

[48]  A Akaike,et al.  Muscarinic inhibition as a dominant role in cholinergic regulation of transmission in the caudate nucleus. , 1988, The Journal of pharmacology and experimental therapeutics.

[49]  J. Penney,et al.  Differential loss of striatal projection neurons in Huntington disease. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[50]  D. James Surmeier,et al.  Voltage-clamp analysis of a transient potassium current in rat neostriatal neurons , 1988, Brain Research.

[51]  H. Kita,et al.  Glutamate decarboxylase immunoreactive neurons in rat neostriatum: their morphological types and populations , 1988, Brain Research.

[52]  C. Wilson,et al.  Relationship of the axonal and dendritic geometry of spiny projection neurons to the compartmental organization of the neostriatum , 1988, The Journal of comparative neurology.

[53]  T Pasik,et al.  GABAergic elements in the neuronal circuits of the monkey neostriatum: A light and electron microscopic immunocytochemical study , 1988, The Journal of comparative neurology.

[54]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[55]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[56]  A. Mcgeorge,et al.  The organization of the projection from the cerebral cortex to the striatum in the rat , 1989, Neuroscience.

[57]  M. Kimura,et al.  Choreic movements in the macaque monkey induced by kainic acid lesions of the striatum combined with L-dopa. Pharmacological, biochemical and physiological studies on neural mechanisms. , 1990, Brain : a journal of neurology.

[58]  M. Kimura Behaviorally contingent property of movement-related activity of the primate putamen. , 1990, Journal of neurophysiology.

[59]  J D Cohen,et al.  A network model of catecholamine effects: gain, signal-to-noise ratio, and behavior. , 1990, Science.

[60]  C. Wilson,et al.  Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[61]  J. Wayne Aldridge,et al.  The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation , 1991, Brain Research.

[62]  N W Kowall,et al.  Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: a combined study using the section-Golgi method and calbindin D28k immunocytochemistry , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Brotchie,et al.  Modeling the functional organization of the basal ganglia. A parallel distributed processing approach , 1991, Movement disorders : official journal of the Movement Disorder Society.

[64]  J. Wickens,et al.  Two dynamic modes of striatal function under dopaminergic‐cholinergic control: Simulation and analysis of a model , 1991, Synapse.

[65]  P. Brotchie,et al.  A neural network model of neural activity in the monkey globus pallidus , 1991, Neuroscience Letters.

[66]  A. Graybiel,et al.  Corticostriatal transformations in the primate somatosensory system. Projections from physiologically mapped body-part representations. , 1991, Journal of neurophysiology.

[67]  N. Yanagisawa The spectrum of motor disorders in Huntington's disease , 1992, Clinical Neurology and Neurosurgery.

[68]  C. Gerfen The neostriatal mosaic: multiple levels of compartmental organization , 1992, Trends in Neurosciences.

[69]  J. Penney,et al.  Preferential loss of striato‐external pallidal projection neurons in presymptomatic Huntington's disease , 1992, Annals of neurology.

[70]  A. Graybiel,et al.  Dendritic arbors of spiny neurons in the primate striatum are directionally polarized , 1993, The Journal of comparative neurology.

[71]  Charles J. Wilson,et al.  The generation of natural firing patterns in neostriatal neurons. , 1993, Progress in brain research.

[72]  J. Wickens,et al.  Analysis of striatal dynamics: the existence of two modes of behaviour. , 1993, Journal of theoretical biology.

[73]  J. Wickens A Theory of the Striatum , 1993 .

[74]  A. Graybiel,et al.  Dendritic domains of medium spiny neurons in the primate striatum: Relationships to striosomal borders , 1993, The Journal of comparative neurology.

[75]  J. Wickens,et al.  The corticostriatal system on computer simulation: an intermediate mechanism for sequencing of actions. , 1993, Progress in brain research.

[76]  D. Plenz,et al.  The Basal Ganglia: “Minimal Coherence Detection” in Cortical Activity Distributions , 1994 .