Factors determining the precision of the correlated firing generated by a monosynaptic connection in the cat visual pathway

Across the visual pathway, strong monosynaptic connections generate a precise correlated firing between presynaptic and postsynaptic neurons. The precision of this correlated firing is not the same within thalamus and visual cortex. While retinogeniculate connections generate a very narrow peak in the correlogram (peak width < 1 ms), the peaks generated by geniculocortical and corticocortical connections have usually a time course of several milliseconds. Several factors could explain these differences in timing precision such as the amplitude of the monosynaptic EPSP (excitatory postsynaptic potential), its time course or the contribution of polysynaptic inputs. While it is difficult to isolate the contribution of each factor in physiological experiments, a first approximation can be done in modelling studies. Here, we simulated two monosynaptically connected neurons to measure changes in their correlated firing as we independently modified different parameters of the connection. Our results suggest that the precision of the correlated firing generated by strong monosynaptic connections is mostly determined by the EPSP time course of the connection and much less by other factors. In addition, we show that a polysynaptic pathway is unlikely to emulate the correlated firing generated by a monosynaptic connection unless it generates EPSPs with very small latency jitter.

[1]  S. Sherman,et al.  Postsynaptic potentials recorded in neurons of the cat's lateral geniculate nucleus following electrical stimulation of the optic chiasm. , 1988, Journal of neurophysiology.

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

[3]  C. Schreiner,et al.  Thalamocortical transformation of responses to complex auditory stimuli , 2004, Experimental Brain Research.

[4]  D. Perkel,et al.  Cooperative firing activity in simultaneously recorded populations of neurons: detection and measurement , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[6]  Ad Aertsen,et al.  Stable propagation of synchronous spiking in cortical neural networks , 1999, Nature.

[7]  A. Aertsen,et al.  Representation of cooperative firing activity among simultaneously recorded neurons. , 1985, Journal of neurophysiology.

[8]  F. J. Veredasa,et al.  A computational tool to simulate correlated activity in neural circuits , 2004 .

[9]  M. Sirota,et al.  Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex. , 1998, Journal of neurophysiology.

[10]  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.

[11]  R. Reid,et al.  Rules of Connectivity between Geniculate Cells and Simple Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[12]  B. B. Lee,et al.  The retinal input to cells in area 17 of the cat's cortex , 1977, Experimental Brain Research.

[13]  J. Eggermont,et al.  Spontaneous burst firing in cat primary auditory cortex: age and depth dependence and its effect on neural interaction measures. , 1993, Journal of neurophysiology.

[14]  U. Eysel,et al.  Quantitative studies of intracellular postsynaptic potentials in the lateral geniculate nucleus of the cat with respect to optic tract stimulus response latencies , 1976, Experimental Brain Research.

[15]  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.

[16]  A. Aertsen,et al.  On the significance of correlations among neuronal spike trains , 2004, Biological Cybernetics.

[17]  J. Lambert,et al.  Somatic amplification of distally generated subthreshold EPSPs in rat hippocampal pyramidal neurones , 1999, The Journal of physiology.

[18]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[19]  W. Levick,et al.  Sustained and transient neurones in the cat's retina and lateral geniculate nucleus , 1971, The Journal of physiology.

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

[21]  Y. Dan,et al.  Temporal Specificity in the Cortical Plasticity of Visual Space Representation , 2002, Science.

[22]  C. Nicholson Electric current flow in excitable cells J. J. B. Jack, D. Noble &R. W. Tsien Clarendon Press, Oxford (1975). 502 pp., £18.00 , 1976, Neuroscience.

[23]  M. Binder,et al.  Functional identification of the input‐output transforms of motoneurones in the rat and cat , 1997, The Journal of physiology.

[24]  D N Mastronarde,et al.  Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive-field properties and classification of cells. , 1987, Journal of neurophysiology.

[25]  K. Tanaka,et al.  Cross-Correlation Analysis of Interneuronal Connectivity in cat visual cortex. , 1981, Journal of neurophysiology.

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

[27]  R. Reid,et al.  Synaptic Integration in Striate Cortical Simple Cells , 1998, The Journal of Neuroscience.

[28]  Stephane A. Roy,et al.  Coincidence Detection or Temporal Integration? What the Neurons in Somatosensory Cortex Are Doing , 2001, The Journal of Neuroscience.

[29]  R. Stein Some models of neuronal variability. , 1967, Biophysical journal.

[30]  S. Yoshizawa,et al.  An Active Pulse Transmission Line Simulating Nerve Axon , 1962, Proceedings of the IRE.

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

[32]  W. Regehr,et al.  Developmental Remodeling of the Retinogeniculate Synapse , 2000, Neuron.

[33]  C. Morris,et al.  Voltage oscillations in the barnacle giant muscle fiber. , 1981, Biophysical journal.

[34]  G L Gerstein,et al.  Mutual temporal relationships among neuronal spike trains. Statistical techniques for display and analysis. , 1972, Biophysical journal.

[35]  B. Gustafsson,et al.  Influence of stretch‐evoked synaptic potentials on firing probability of cat spinal motoneurones. , 1984, The Journal of physiology.

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

[37]  E. Fetz,et al.  Synaptic Interactions between Primate Precentral Cortex Neurons Revealed by Spike-Triggered Averaging of Intracellular Membrane Potentials In Vivo , 1996, The Journal of Neuroscience.

[38]  S. Sherman,et al.  Structure of physiologically identified X and Y cells in the cat's lateral geniculate nucleus. , 1979, Science.

[39]  C. Brody Slow covariations in neuronal resting potentials can lead to artefactually fast cross-correlations in their spike trains. , 1998, Journal of neurophysiology.

[40]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[41]  R. Reid,et al.  Low Response Variability in Simultaneously Recorded Retinal, Thalamic, and Cortical Neurons , 2000, Neuron.

[42]  E E Fetz,et al.  Cross‐correlation assessment of synaptic strength of single Ia fibre connections with triceps surae motoneurones in cats. , 1987, The Journal of physiology.

[43]  A. Aertsen,et al.  Neuronal Integration of Synaptic Input in the Fluctuation-Driven Regime , 2004, The Journal of Neuroscience.

[44]  W. Singer,et al.  Stimulus‐Dependent Neuronal Oscillations in Cat Visual Cortex: Receptive Field Properties and Feature Dependence , 1990, The European journal of neuroscience.

[45]  T. Sears,et al.  The effects of single afferent impulses on the probability of firing of external intercostal motoneurones in the cat , 1982, The Journal of physiology.

[46]  Richard Miles,et al.  EPSP Amplification and the Precision of Spike Timing in Hippocampal Neurons , 2000, Neuron.

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

[48]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[49]  B. Sakmann,et al.  Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons , 1995, Neuron.

[50]  R. Reid,et al.  Temporal Coding of Visual Information in the Thalamus , 2000, The Journal of Neuroscience.

[51]  C. Knox,et al.  Cross-correlation functions for a neuronal model. , 1974, Biophysical journal.

[52]  Interactions among an ensemble of chordotonal organ receptors and motor neurons of the crayfish claw. , 1979, Journal of neurophysiology.

[53]  B. Knight,et al.  Response variability and timing precision of neuronal spike trains in vivo. , 1997, Journal of neurophysiology.

[54]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[55]  A. Zador,et al.  Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex , 2003, Nature.

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

[57]  B Sakmann,et al.  Synaptic efficacy and reliability of excitatory connections between the principal neurones of the input (layer 4) and output layer (layer 5) of the neocortex , 2000, The Journal of physiology.

[58]  J. Alonso,et al.  Functional connectivity between simple cells and complex cells in cat striate cortex , 1998, Nature Neuroscience.

[59]  P. Kirkwood On the use and interpretation of cross-correlation measurements in the mammalian central nervous system , 1979, Journal of Neuroscience Methods.

[60]  A. Reyes,et al.  Two modes of interspike interval shortening by brief transient depolarizations in cat neocortical neurons. , 1993, Journal of neurophysiology.

[61]  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.

[62]  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.

[63]  H. Swadlow,et al.  Activation of a Cortical Column by a Thalamocortical Impulse , 2002, The Journal of Neuroscience.

[64]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[65]  D. James Surmeier,et al.  The relationship between cross-correlation measures and underlying synaptic events , 1985, Brain Research.

[66]  Bert Sakmann,et al.  Monosynaptic Connections between Pairs of Spiny Stellate Cells in Layer 4 and Pyramidal Cells in Layer 5A Indicate That Lemniscal and Paralemniscal Afferent Pathways Converge in the Infragranular Somatosensory Cortex , 2005, The Journal of Neuroscience.

[67]  D. Ferster,et al.  An intracellular analysis of geniculo‐cortical connectivity in area 17 of the cat. , 1983, The Journal of physiology.

[68]  H. Swadlow,et al.  Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. , 1995, Journal of neurophysiology.

[69]  Robert Shapley,et al.  Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction velocities of their inputs , 1979, Experimental Brain Research.

[70]  Jessy D. Dorn,et al.  Estimating membrane voltage correlations from extracellular spike trains. , 2003, Journal of neurophysiology.

[71]  B. Connors,et al.  Two networks of electrically coupled inhibitory neurons in neocortex , 1999, Nature.

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

[73]  R. Silver,et al.  Synaptic connections between layer 4 spiny neurone‐ layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column , 2002, The Journal of physiology.

[74]  C. Shatz,et al.  Synaptic Activity and the Construction of Cortical Circuits , 1996, Science.

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

[76]  D. Debanne,et al.  Long‐term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures , 1998, The Journal of physiology.

[77]  Heinke,et al.  Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons , 2022 .

[78]  E E Fetz,et al.  Relation between shapes of post‐synaptic potentials and changes in firing probability of cat motoneurones , 1983, The Journal of physiology.

[79]  R. FitzHugh Impulses and Physiological States in Theoretical Models of Nerve Membrane. , 1961, Biophysical journal.

[80]  R. Stein,et al.  The information capacity of nerve cells using a frequency code. , 1967, Biophysical journal.

[81]  Y. Dan,et al.  Spike-timing-dependent synaptic modification induced by natural spike trains , 2002, Nature.

[82]  W. Levick,et al.  Simultaneous recording of input and output of lateral geniculate neurones. , 1971, Nature: New biology.

[83]  W. Levick,et al.  Lateral geniculate neurons of cat: retinal inputs and physiology. , 1972, Investigative ophthalmology.

[84]  G. P. Moore,et al.  Statistical signs of synaptic interaction in neurons. , 1970, Biophysical journal.

[85]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[86]  J. M. Alonso,et al.  A computational tool to simulate correlated activity in neural circuits , 2004, Journal of Neuroscience Methods.

[87]  Bruce W. Knight,et al.  Dynamics of Encoding in a Population of Neurons , 1972, The Journal of general physiology.

[88]  Lee M. Miller,et al.  Functional Convergence of Response Properties in the Auditory Thalamocortical System , 2001, Neuron.

[89]  C. Gray,et al.  Adaptive Coincidence Detection and Dynamic Gain Control in Visual Cortical Neurons In Vivo , 2003, Neuron.

[90]  M. Scanziani,et al.  Enforcement of Temporal Fidelity in Pyramidal Cells by Somatic Feed-Forward Inhibition , 2001, Science.

[91]  S. Hestrin,et al.  A network of fast-spiking cells in the neocortex connected by electrical synapses , 1999, Nature.

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

[93]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[94]  Nikolai Axmacher,et al.  Intrinsic cellular currents and the temporal precision of EPSP–action potential coupling in CA1 pyramidal cells , 2004, The Journal of physiology.

[95]  S. Sherman,et al.  Synaptic circuits involving an individual retinogeniculate axon in the cat , 1987, The Journal of comparative neurology.

[96]  E. Bienenstock,et al.  Theory for the development of neuron selectivity: orientation specificity and binocular interaction in visual cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.