Synaptic Interactions between Thalamic Inputs to Simple Cells in Cat Visual Cortex

We performed experiments in the cat geniculocortical pathway,in vivo, to examine how presynaptic spikes interact to influence the firing of postsynaptic targets. In particular, we asked (1) how do multiple spikes from a single presynaptic neuron interact to influence the firing of a postsynaptic target (homosynaptic interactions), (2) how do spikes from two different presynaptic neurons interact (heterosynaptic interactions), and (3) what is the time course of homosynaptic and heterosynaptic interactions? We found that both homosynaptic and heterosynaptic interactions increase the likelihood of driving a postsynaptic spike, although with different time courses. For two spikes traveling down a single geniculate axon, the second spike is more effective than the first for ∼15 msec. For two spikes on separate axons, the interaction is faster (∼7 msec duration, ∼2.5 msec time constant). Thus changes in firing rate are perhaps best relayed by homosynaptic interactions, whereas heterosynaptic interactions may help detect coincident spikes from different thalamic inputs.

[1]  D. Hubel.  Tungsten Microelectrode for Recording from Single Units. , 1957, Science.

[2]  D. Hubel,et al.  Integrative action in the cat's lateral geniculate body , 1961, The Journal of physiology.

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

[4]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. I. The single spike train. , 1967, Biophysical journal.

[5]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[6]  M. C. Citron,et al.  Spatial and temporal receptive-field analysis of the cats geniculocortical pathway , 1981, Vision Research.

[7]  R C Emerson,et al.  Spatial and temporal receptive-field analysis of the cat's geniculocortical pathway. , 1981, Vision research.

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

[9]  Keiji Tanaka.  Organization of geniculate inputs to visual cortical cells in the cat , 1985, Vision Research.

[10]  J. P. Jones,et al.  The two-dimensional spatial structure of simple receptive fields in cat striate cortex. , 1987, Journal of neurophysiology.

[11]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. , 1987, Journal of neurophysiology.

[12]  Ee Sutter,et al.  A deterministic approach to nonlinear systems analysis , 1992 .

[13]  R. Shapley,et al.  Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex , 1992, Visual Neuroscience.

[14]  R. B. Pinter,et al.  Nonlinear Vision: Determination of Neural Receptive Fields, Function, and Networks , 1992 .

[15]  R. Eckhorn,et al.  A new method for the insertion of multiple microprobes into neural and muscular tissue, including fiber electrodes, fine wires, needles and microsensors , 1993, Journal of Neuroscience Methods.

[16]  George L. Gerstein,et al.  Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex , 1994, Nature.

[17]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

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

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

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

[21]  J. Movshon,et al.  Spike train encoding by regular-spiking cells of the visual cortex. , 1996, Journal of neurophysiology.

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

[23]  S. Sherman,et al.  Dual response modes in lateral geniculate neurons: Mechanisms and functions , 1996, Visual Neuroscience.

[24]  W. Singer,et al.  Integrator or coincidence detector? The role of the cortical neuron revisited , 1996, Trends in Neurosciences.

[25]  W. Regehr,et al.  Timing of neurotransmission at fast synapses in the mammalian brain , 1996, Nature.

[26]  C. Koch,et al.  A brief history of time (constants). , 1996, Cerebral cortex.

[27]  R. Reid,et al.  Precisely correlated firing in cells of the lateral geniculate nucleus , 1996, Nature.

[28]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[29]  C. Stevens,et al.  Very short-term plasticity in hippocampal synapses. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[30]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Maria V. Sanchez-Vives,et al.  Influence of low and high frequency inputs on spike timing in visual cortical neurons. , 1997, Cerebral cortex.

[32]  R. Shapley,et al.  The use of m-sequences in the analysis of visual neurons: Linear receptive field properties , 1997, Visual Neuroscience.

[33]  B. Sakmann,et al.  Calcium action potentials restricted to distal apical dendrites of rat neocortical pyramidal neurons , 1997, The Journal of physiology.

[34]  L. Abbott,et al.  A Quantitative Description of Short-Term Plasticity at Excitatory Synapses in Layer 2/3 of Rat Primary Visual Cortex , 1997, The Journal of Neuroscience.

[35]  W. Singer,et al.  Modification of discharge patterns of neocortical neurons by induced oscillations of the membrane potential , 1998, Neuroscience.

[36]  R. Reid,et al.  Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus , 1998, Nature.

[37]  Y. Dan,et al.  Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus , 1998, Nature Neuroscience.

[38]  Reid R. Clay,et al.  Specificity and strength of retinogeniculate connections. , 1999, Journal of neurophysiology.

[39]  J. A. Varela,et al.  Differential Depression at Excitatory and Inhibitory Synapses in Visual Cortex , 1999, The Journal of Neuroscience.

[40]  R. Reid,et al.  Synchronous activity in the visual system. , 1999, Annual review of physiology.

[41]  C. Stevens,et al.  Response of Hippocampal Synapses to Natural Stimulation Patterns , 1999, Neuron.

[42]  C. Koch,et al.  Encoding of visual information by LGN bursts. , 1999, Journal of neurophysiology.

[43]  W G Regehr,et al.  Timing of synaptic transmission. , 1999, Annual review of physiology.

[44]  B. Connors,et al.  Efficacy of Thalamocortical and Intracortical Synaptic Connections Quanta, Innervation, and Reliability , 1999, Neuron.

[45]  Microsaccadic eye movements and firing of single cells in the striate cortex of macaque monkeys , 2000, Nature Neuroscience.

[46]  C. Gray,et al.  Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[47]  R C Reid,et al.  Divergence and reconvergence: multielectrode analysis of feedforward connections in the visual system. , 2001, Progress in brain research.

[48]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[49]  R. Clay Reid,et al.  Integration of Thalamic Inputs to Cat Primary Visual Cortex , 2002 .