The role of synapses in cortical computation

SummaryThe synapse, first introduced as a physiological hypothesis by C. S. Sherrington at the close of the nineteenth century, has, 100 years on, become the nexus for anatomical and functional investigations of interneuronal communication. A number of hypotheses have been proposed that give local synaptic interactions specific roles in generating an algebra or logic for computations in the neocortex. Experimental work, however, has provided little support for such schemes. Instead, both structural and functional studies indicate that characteristically cortical functions, e. g., the identification of the motion or orientation of objects, involve computations that must be achieved with high accuracy through the collective action of hundreds or thousands of neurons connected in recurrent microcircuits. Some important principles that emerge from this collective action can effectively be captured by simple electronic models. More detailed models explain the nature of the complex computations performed by the cortical circuits and how the computations remain so remarkably robust in the face of a number of sources of noise, including variability in the anatomical connections, large variance in the synaptic responses and in the tria-to-trial output of single neurons, and weak or degraded input signals.

[1]  K. Uchizono Characteristics of Excitatory and Inhibitory Synapses in the Central Nervous System of the Cat , 1965, Nature.

[2]  K. Martin,et al.  The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. , 1988, Quarterly journal of experimental physiology.

[3]  T. Poggio,et al.  The synaptic veto mechanism: does it underlie direction and orientation selectivity in the visual cortex , 1985 .

[4]  J. Jack,et al.  Electric current flow in excitable cells , 1975 .

[5]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[6]  B W Connors,et al.  Inhibitory control of excitable dendrites in neocortex. , 1995, Journal of neurophysiology.

[7]  S. Cajal Recollections of my life , 1989 .

[8]  K. Tanaka Cross-correlation analysis of geniculostriate neuronal relationships in cats. , 1983, Journal of neurophysiology.

[9]  T. Poggio,et al.  Biophysics of Computation: Neurons, Synapses and Membranes , 1984 .

[10]  W. Denk,et al.  Dendritic spines as basic functional units of neuronal integration , 1995, Nature.

[11]  A. Peters,et al.  A new procedure for examining Golgi impregnated neurons by light and electron microscopy , 1977, Journal of neurocytology.

[12]  M. McDonald,et al.  A re‐appraisal of the role of marketing planning , 1987 .

[13]  D. Whitteridge,et al.  Mechanisms of inhibition in cat visual cortex. , 1991, The Journal of physiology.

[14]  T. Blackstad,et al.  Electron microscopy of experimental axonal degeneration in photochemically modified golgi preparations: A procedure for precise mapping of nervous connections , 1975, Brain Research.

[15]  T. Teyler,et al.  Long-term potentiation. , 1987, Annual review of neuroscience.

[16]  I. Ohzawa,et al.  Stereoscopic depth discrimination in the visual cortex: neurons ideally suited as disparity detectors. , 1990, Science.

[17]  B. Gustafsson,et al.  Long-term potentiation in the hippocampus using depolarizing current pulses as the conditioning stimulus to single volley synaptic potentials , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[18]  C. Koch,et al.  Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  D Ferster,et al.  Synaptic excitation of neurones in area 17 of the cat by intracortical axon collaterals of cortico‐geniculate cells. , 1985, The Journal of physiology.

[20]  Gray Eg Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study , 1959 .

[21]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  C. Gilbert,et al.  Laminar patterns of geniculocortical projection in the cat , 1976, Brain Research.

[23]  B. L. Ginsborg THE PHYSIOLOGY OF SYNAPSES , 1964 .

[24]  L. Garey A light and electron microscopic study of the visual cortex of the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[25]  D. Ferster Spatially opponent excitation and inhibition in simple cells of the cat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[27]  G. M. Shepherd,et al.  The neuron doctrine: a revision of functional concepts. , 1972, The Yale journal of biology and medicine.

[28]  T. Bonhoeffer,et al.  Functional topography of horizontal neuronal networks in cat visual cortex (area 18) , 1996 .

[29]  J J Jack,et al.  Quantal analysis of excitatory synaptic mechanisms in the mammalian central nervous system. , 1990, Cold Spring Harbor symposia on quantitative biology.

[30]  T. Powell,et al.  An experimental study of the termination of the lateral geniculo–cortical pathway in the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[31]  G. Major,et al.  The modelling of pyramidal neurones in the visual cortex , 1989 .

[32]  R. Douglas,et al.  A functional microcircuit for cat visual cortex. , 1991, The Journal of physiology.

[33]  J. C. Anderson,et al.  Polyneuronal innervation of spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[34]  G. Shepherd,et al.  Logic operations are properties of computer-simulated interactions between excitable dendritic spines , 1987, Neuroscience.

[35]  A Meyer,et al.  Boutons terminaux in the cerebral cortex. , 1945, Journal of anatomy.

[36]  K. Martin Neuronal Circuits in Cat Striate Cortex , 1984 .

[37]  E. Gray,et al.  Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. , 1959, Journal of anatomy.

[38]  B. Katz,et al.  The effect of inhibitory nerve impulses on a crustacean muscle fibre , 1953, The Journal of physiology.

[39]  S. Nelson,et al.  An emergent model of orientation selectivity in cat visual cortical simple cells , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  Prof. Dr. Valentino Braitenberg,et al.  Anatomy of the Cortex , 1991, Studies of Brain Function.

[41]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[42]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[43]  T. Wiesel,et al.  Patterns of synaptic input to layer 4 of cat striate cortex , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  S. Blomfield Arithmetical operations performed by nerve cells. , 1974, Brain research.

[45]  T. Sejnowski,et al.  [Letters to nature] , 1996, Nature.

[46]  J. C. Anderson,et al.  Map of the synapses formed with the dendrites of spiny stellate neurons of cat visual cortex , 1994, The Journal of comparative neurology.

[47]  F. Valverde Short axon neuronal subsystems in the visual cortex of the monkey. , 1971, The International journal of neuroscience.

[48]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[49]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[50]  Idan Segev,et al.  Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Bartlett W. Mel Synaptic integration in an excitable dendritic tree. , 1993, Journal of neurophysiology.

[52]  D. Prince,et al.  Sodium channels in dendrites of rat cortical pyramidal neurons. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Bartlett W. Mel,et al.  Information Processing in Dendritic Trees , 1994, Neural Computation.

[54]  C. G. Phillips,et al.  Actions of antidromic pyramidal volleys on single Betz cells in the cat. , 1959, Quarterly journal of experimental physiology and cognate medical sciences.

[55]  R. Clay Reid,et al.  Visually evoked calcium action potentials in cat striate cortex , 1995, Nature.

[56]  T. Poggio,et al.  Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[57]  J F Fulton,et al.  Physiology of the Nervous System , 1939, Science.

[58]  David Hubel,et al.  A big step along the visual pathway , 1996, Nature.

[59]  D. Whitteridge,et al.  Selective responses of visual cortical cells do not depend on shunting inhibition , 1988, Nature.

[60]  A. Peters,et al.  Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. , 1993, Cerebral cortex.

[61]  D Ferster,et al.  Augmenting responses evoked in area 17 of the cat by intracortical axon collaterals of cortico‐geniculate cells. , 1985, The Journal of physiology.

[62]  K. Martin,et al.  Excitatory synaptic inputs to spiny stellate cells in cat visual cortex , 1996, Nature.

[63]  C. Sherrington Man On His Nature , 1940 .

[64]  J. Lund Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatta) , 1973, The Journal of comparative neurology.

[65]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[66]  C. Sherrington Integrative Action of the Nervous System , 1907 .

[67]  Peter Sterling,et al.  Ultrastructure of synapses from the A‐laminae of the lateral geniculate nucleus in layer IV of the cat striate cortex , 1987, The Journal of comparative neurology.

[68]  D. Ferster,et al.  Orientation selectivity of thalamic input to simple cells of cat visual cortex , 1996, Nature.

[69]  D. Hubel,et al.  Receptive fields of single neurones in the cat's striate cortex , 1959, The Journal of physiology.

[70]  J Bullier,et al.  Receptive-field transformations between LGN neurons and S-cells of cat-striate cortex. , 1982, Journal of neurophysiology.

[71]  H. Markram,et al.  Calcium transients in dendrites of neocortical neurons evoked by single subthreshold excitatory postsynaptic potentials via low-voltage-activated calcium channels. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[72]  D. Whitteridge,et al.  Innervation of cat visual areas 17 and 18 by physiologically identified X‐ and Y‐ type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation , 1985, The Journal of comparative neurology.

[73]  W. R. Adey The synaptic organization of the brain. 2nd edn. , 1981 .

[74]  D. Hubel,et al.  Ferrier lecture - Functional architecture of macaque monkey visual cortex , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[75]  J. Eccles The Ferrier Lecture: The nature of central inhibition , 1961, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[76]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

[77]  J C Anderson,et al.  Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex , 1994, The Journal of comparative neurology.

[78]  G. Shepherd Microcircuits in the nervous system. , 1978, Scientific American.

[79]  J. Szentágothai Synaptology of the Visual Cortex , 1973 .

[80]  O D Creutzfeldt,et al.  Whole cell recording and conductance measurements in cat visual cortex in-vivo. , 1991, Neuroreport.

[81]  P. Brodal The Central Nervous System , 1992 .

[82]  C. Koch,et al.  Amplification and linearization of distal synaptic input to cortical pyramidal cells. , 1994, Journal of neurophysiology.

[83]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[84]  Charles Scott Sherrington Reciprocal Innervation of Antagonistic Muscles. Thirteenth Note.-On the Antagonism between Reflex Inhibition and Reflex Excitation , 1908 .

[85]  H. Pockberger,et al.  Electrophysiological and morphological properties of rat motor cortex neurons in vivo , 1991, Brain Research.

[86]  C. Koch,et al.  Synaptic background activity influences spatiotemporal integration in single pyramidal cells. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[87]  C. Koch,et al.  Recurrent excitation in neocortical circuits , 1995, Science.

[88]  Kevan A. C. Martin,et al.  Hybrid analog-digital architectures for neuromorphic systems , 1994, Proceedings of 1994 IEEE International Conference on Neural Networks (ICNN'94).

[89]  A. Das,et al.  Orientation in Visual Cortex: A Simple Mechanism Emerges , 1996, Neuron.

[90]  K. Martin,et al.  Excitation by geniculocortical synapses is not ‘vetoed’ at the level of dendritic spines in cat visual cortex. , 1991, The Journal of physiology.

[91]  H. Barlow,et al.  The mechanism of directionally selective units in rabbit's retina. , 1965, The Journal of physiology.

[92]  R. Reid,et al.  Specificity of monosynaptic connections from thalamus to visual cortex , 1995, Nature.

[93]  Kevan A. C. Martin,et al.  A Canonical Microcircuit for Neocortex , 1989, Neural Computation.

[94]  E. G. Jones,et al.  Varieties and distribution of non‐pyramidal cells in the somatic sensory cortex of the squirrel monkey , 1975, The Journal of comparative neurology.

[95]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

[96]  S. Levay,et al.  Synaptic organization of claustral and geniculate afferents to the visual cortex of the cat , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[97]  S. Levay,et al.  Synaptic patterns in the visual cortex of the cat and monkey. Electron microscopy of Golgi Preparations , 1973, The Journal of comparative neurology.

[98]  D. Ferster,et al.  EPSP-IPSP interactions in cat visual cortex studied with in vivo whole- cell patch recording , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.