Adaptive Integration in the Visual Cortex by Depressing Recurrent Cortical Circuits

Neurons in the visual cortex receive a large amount of input from recurrent connections, yet the functional role of these connections remains unclear. Here we explore networks with strong recurrence in a computational model and show that short-term depression of the synapses in the recurrent loops implements an adaptive filter. This allows the visual system to respond reliably to deteriorated stimuli yet quickly to high-quality stimuli. For low-contrast stimuli, the model predicts long response latencies, whereas latencies are short for high-contrast stimuli. This is consistent with physiological data showing that in higher visual areas, latencies can increase more than 100 ms at low contrast compared to high contrast. Moreover, when presented with briefly flashed stimuli, the model predicts stereotypical responses that outlast the stimulus, again consistent with physiological findings. The adaptive properties of the model suggest that the abundant recurrent connections found in visual cortex serve to adapt the network's time constant in accordance with the stimulus and normalizes neuronal signals such that processing is as fast as possible while maintaining reliability.

[1]  Frances S. Chance,et al.  Synaptic Depression and the Temporal Response Characteristics of V1 Cells , 1998, The Journal of Neuroscience.

[2]  Mark C. W. van Rossum,et al.  Fast Propagation of Firing Rates through Layered Networks of Noisy Neurons , 2002, The Journal of Neuroscience.

[3]  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.

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

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

[6]  C. Gilbert,et al.  Synaptic physiology of horizontal connections in the cat's visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[8]  A. Thomson,et al.  Fluctuations in pyramid-pyramid excitatory postsynaptic potentials modified by presynaptic firing pattern and postsynaptic membrane potential using paired intracellular recordings in rat neocortex , 1993, Neuroscience.

[9]  Peter Földiák,et al.  Modelling spike trains and extracting response latency with Bayesian binning , 2010, Journal of Physiology-Paris.

[10]  A. Saul Adaptation aftereffects in single neurons of cat visual cortex: Response timing is retarded by adapting , 1995, Visual Neuroscience.

[11]  A. Treves Mean-field analysis of neuronal spike dynamics , 1993 .

[12]  D. G. Albrecht,et al.  Striate cortex of monkey and cat: contrast response function. , 1982, Journal of neurophysiology.

[13]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[14]  K. Miller,et al.  Neural noise can explain expansive, power-law nonlinearities in neural response functions. , 2002, Journal of neurophysiology.

[15]  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.

[16]  D. Hansel,et al.  How Noise Contributes to Contrast Invariance of Orientation Tuning in Cat Visual Cortex , 2002, The Journal of Neuroscience.

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

[18]  Nicholas J. Priebe,et al.  Contrast-dependent nonlinearities arise locally in a model of contrast-invariant orientation tuning. , 2001, Journal of neurophysiology.

[19]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[20]  J. Movshon,et al.  The Timing of Response Onset and Offset in Macaque Visual Neurons , 2002, The Journal of Neuroscience.

[21]  A. Destexhe,et al.  Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. , 1999, Journal of neurophysiology.

[22]  Henry Markram,et al.  Neural Networks with Dynamic Synapses , 1998, Neural Computation.

[23]  B J Richmond,et al.  Stochastic nature of precisely timed spike patterns in visual system neuronal responses. , 1999, Journal of neurophysiology.

[24]  Pieter R Roelfsema,et al.  Subtask sequencing in the primary visual cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Wulfram Gerstner,et al.  Population Dynamics of Spiking Neurons: Fast Transients, Asynchronous States, and Locking , 2000, Neural Computation.

[26]  B. Richmond,et al.  Latency: another potential code for feature binding in striate cortex. , 1996, Journal of neurophysiology.

[27]  M. Tovée,et al.  Processing speed in the cerebral cortex and the neurophysiology of visual masking , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  Tim P Vogels,et al.  Signal Propagation and Logic Gating in Networks of Integrate-and-Fire Neurons , 2005, The Journal of Neuroscience.

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

[30]  D. Ferster,et al.  The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. , 2000, Science.

[31]  D. G. Albrecht Visual cortex neurons in monkey and cat: Effect of contrast on the spatial and temporal phase transfer functions , 1995, Visual Neuroscience.

[32]  M. Carandini,et al.  Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. , 2000, Journal of neurophysiology.

[33]  K. Obermayer,et al.  The Role of Feedback in Shaping the Extra-Classical Receptive Field of Cortical Neurons: A Recurrent Network Model , 2006, The Journal of Neuroscience.

[34]  D. Tolhurst,et al.  Factors influencing the temporal phase of response to bar and grating stimuli for simple cells in the cat striate cortex , 2004, Experimental Brain Research.

[35]  C. Levelt,et al.  Contrast gain control and cortical TrkB signaling shape visual acuity , 2010, Nature Neuroscience.

[36]  M W Oram,et al.  The temporal resolution of neural codes: does response latency have a unique role? , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[37]  Nicholas J. Priebe,et al.  Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex , 2005, The Journal of Neuroscience.

[38]  R. Douglas,et al.  An intracellular study of the contrast-dependence of neuronal activity in cat visual cortex. , 1997, Cerebral cortex.

[39]  V. Bringuier,et al.  Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. , 1999, Science.

[40]  M. Oram Contrast induced changes in response latency depend on stimulus specificity , 2010, Journal of Physiology-Paris.

[41]  Misha Tsodyks,et al.  Computation by Ensemble Synchronization in Recurrent Networks with Synaptic Depression , 2002, Journal of Computational Neuroscience.

[42]  J Gautrais,et al.  Rate coding versus temporal order coding: a theoretical approach. , 1998, Bio Systems.

[43]  V Virsu,et al.  Phase of responses to moving sinusoidal gratings in cells of cat retina and lateral geniculate nucleus. , 1981, Journal of neurophysiology.

[44]  G. Orban,et al.  Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. , 1999, Journal of neurophysiology.

[45]  D. I. Perrett,et al.  Out of sight but not out of mind: the neurophysiology of iconic memory in the superior temporal sulcus , 2005, Cognitive neuropsychology.

[46]  Dominik Endres,et al.  Feature extraction from spike trains with Bayesian binning: ‘Latency is where the signal starts’ , 2010, Journal of Computational Neuroscience.

[47]  M Vanrossum Computation with populations codes in layered networks of integrate-and-fire neurons , 2004 .

[48]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[49]  Robert A. Frazor,et al.  Visual cortex neurons of monkeys and cats: temporal dynamics of the contrast response function. , 2002, Journal of neurophysiology.

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

[51]  Mark C. W. van Rossum,et al.  Computation with populations codes in layered networks of integrate-and-fire neurons , 2004, Neurocomputing.

[52]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[53]  Barry J. Richmond,et al.  Consistency of Encoding in Monkey Visual Cortex , 2001, The Journal of Neuroscience.

[54]  Guido Bugmann,et al.  A Model for Latencies in the Visual System , 1993 .

[55]  M. Carandini,et al.  A Synaptic Explanation of Suppression in Visual Cortex , 2002, The Journal of Neuroscience.

[56]  D. Perrett,et al.  Time course of neural responses discriminating different views of the face and head. , 1992, Journal of neurophysiology.

[57]  Mark C. W. van Rossum,et al.  Recurrent networks with short term synaptic depression , 2009, Journal of Computational Neuroscience.