Gain modulation of neuronal responses by subtractive and divisive mechanisms of inhibition.

Gain modulation of neuronal responses is widely observed in the cerebral cortex of both anesthetized and behaving animals. Does this multiplicative effect on neuronal tuning curves require underlying multiplicative mechanisms of integration? We compare the effects of a divisive mechanism of inhibition (noisy excitatory and inhibitory synaptic inputs) with the effects of two subtractive mechanisms (shunting conductance and hyperpolarizing current) on the tuning curves of a model cortical neuron. We find that, although the effects of subtractive inhibition can appear nonlinear, they are accompanied by a change in response threshold and are best described as a vertical shift along the response axis. Increasing noisy synaptic activity divisively scales the model responses, reproducing a response-gain control effect. When mutual inhibition between subpopulations of local neurons is included, the model exhibits a gain modulation effect that is better described as input-gain control. We apply these findings to experimental data by examining how noisy synaptic input may underlie divisive surround suppression and attention-driven gain modulation of neuronal responses in the visual system.

[1]  K. Naka,et al.  S‐potentials from luminosity units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[2]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[3]  B. Dreher.  Hypercomplex cells in the cat's striate cortex. , 1972, Investigative ophthalmology.

[4]  B. Finlay,et al.  Short-term response variability of monkey striate neurons , 1976, Brain Research.

[5]  J. Nelson,et al.  Orientation-selective inhibition from beyond the classic visual receptive field , 1978, Brain Research.

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

[7]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[8]  J. Allman,et al.  Stimulus specific responses from beyond the classical receptive field: neurophysiological mechanisms for local-global comparisons in visual neurons. , 1985, Annual review of neuroscience.

[9]  H. Spitzer,et al.  Increased attention enhances both behavioral and neuronal performance. , 1988, Science.

[10]  T. Wiesel,et al.  The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat , 1990, Vision Research.

[11]  P. Lennie,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[12]  D. Tolhurst,et al.  Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex , 1991, Visual Neuroscience.

[13]  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.

[14]  D. Heeger.  Normalization of cell responses in cat striate cortex , 1992, Visual Neuroscience.

[15]  D. Heeger.  Modeling simple-cell direction selectivity with normalized, half-squared, linear operators. , 1993, Journal of neurophysiology.

[16]  William R. Softky,et al.  The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  I. Ohzawa,et al.  Length and width tuning of neurons in the cat's primary visual cortex. , 1994, Journal of neurophysiology.

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

[19]  H. Jones,et al.  Visual cortical mechanisms detecting focal orientation discontinuities , 1995, Nature.

[20]  William R. Softky,et al.  Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. , 1996, Journal of neurophysiology.

[21]  J. Movshon,et al.  Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex , 1997, The Journal of Neuroscience.

[22]  J. B. Levitt,et al.  Contrast dependence of contextual effects in primate visual cortex , 1997, nature.

[23]  Christof Koch,et al.  Shunting Inhibition Does Not Have a Divisive Effect on Firing Rates , 1997, Neural Computation.

[24]  D. Heeger,et al.  Contrast normalization and a linear model for the directional selectivity of simple cells in cat striate cortex , 1997, Visual Neuroscience.

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

[26]  A. Destexhe,et al.  Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo. , 1998, Journal of neurophysiology.

[27]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

[28]  Carrie J. McAdams,et al.  Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4 , 1999, The Journal of Neuroscience.

[29]  R. Desimone,et al.  The Role of Neural Mechanisms of Attention in Solving the Binding Problem , 1999, Neuron.

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

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

[32]  R. Desimone,et al.  Attention Increases Sensitivity of V4 Neurons , 2000, Neuron.

[33]  Emilio Salinas,et al.  Gain Modulation A Major Computational Principle of the Central Nervous System , 2000, Neuron.

[34]  Brent Doiron,et al.  Subtractive and Divisive Inhibition: Effect of Voltage-Dependent Inhibitory Conductances and Noise , 2001, Neural Computation.

[35]  R. Shapley,et al.  Visual spatial characterization of macaque V1 neurons. , 2001, Journal of neurophysiology.

[36]  D. Ferster,et al.  Membrane Potential and Conductance Changes Underlying Length Tuning of Cells in Cat Primary Visual Cortex , 2001, The Journal of Neuroscience.

[37]  S. Treue.  Neural correlates of attention in primate visual cortex , 2001, Trends in Neurosciences.

[38]  S. Treue,et al.  Attentional Modulation Strength in Cortical Area MT Depends on Stimulus Contrast , 2002, Neuron.

[39]  Frances S. Chance,et al.  Gain Modulation from Background Synaptic Input , 2002, Neuron.

[40]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[41]  L. Palmer,et al.  Effects of surround motion on receptive-field gain and structure in area 17 of the cat , 2002, Visual Neuroscience.

[42]  J. Movshon,et al.  Selectivity and spatial distribution of signals from the receptive field surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[43]  R. Silver,et al.  Shunting Inhibition Modulates Neuronal Gain during Synaptic Excitation , 2003, Neuron.

[44]  Andrea Hasenstaub,et al.  Barrages of Synaptic Activity Control the Gain and Sensitivity of Cortical Neurons , 2003, The Journal of Neuroscience.

[45]  Kenneth D Miller,et al.  Multiplicative Gain Changes Are Induced by Excitation or Inhibition Alone , 2003, The Journal of Neuroscience.

[46]  L. Palmer,et al.  Response to Contrast of Electrophysiologically Defined Cell Classes in Primary Visual Cortex , 2003, The Journal of Neuroscience.

[47]  Lyle J. Graham,et al.  Orientation and Direction Selectivity of Synaptic Inputs in Visual Cortical Neurons A Diversity of Combinations Produces Spike Tuning , 2003, Neuron.

[48]  D. McCormick,et al.  Turning on and off recurrent balanced cortical activity , 2003, Nature.

[49]  T. Sejnowski,et al.  Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity , 2003, Neuroscience.

[50]  D. Ulrich.  Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells , 2003, The European journal of neuroscience.

[51]  S. Prescott,et al.  Gain control of firing rate by shunting inhibition: Roles of synaptic noise and dendritic saturation , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  S. Treue,et al.  Feature-Based Attention Increases the Selectivity of Population Responses in Primate Visual Cortex , 2004, Current Biology.

[53]  O. Creutzfeldt,et al.  The representation of contrast and other stimulus parameters by single neurons in area 17 of the cat , 1984, Pflügers Archiv.

[54]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[55]  P. Heggelund,et al.  Response variability and orientation discrimination of single cells in striate cortex of cat , 1978, Experimental Brain Research.

[56]  P. H. Schiller,et al.  State dependent activity in monkey visual cortex , 2004, Experimental Brain Research.

[57]  G. Orban,et al.  The response variability of striate cortical neurons in the behaving monkey , 2004, Experimental Brain Research.

[58]  J. Nelson,et al.  Intracortical facilitation among co-oriented, co-axially aligned simple cells in cat striate cortex , 2004, Experimental Brain Research.

[59]  H. Ozeki,et al.  Relationship between Excitation and Inhibition Underlying Size Tuning and Contextual Response Modulation in the Cat Primary Visual Cortex , 2004, The Journal of Neuroscience.

[60]  J. Reynolds,et al.  Attentional modulation of visual processing. , 2004, Annual review of neuroscience.

[61]  M. Sur,et al.  Invariant computations in local cortical networks with balanced excitation and inhibition , 2005, Nature Neuroscience.

[62]  J. Maunsell,et al.  Effects of spatial attention on contrast response functions in macaque area V4. , 2006, Journal of neurophysiology.

[63]  R. Freeman,et al.  Origins of cross-orientation suppression in the visual cortex. , 2006, Journal of neurophysiology.

[64]  Nicholas J. Priebe,et al.  The Emergence of Contrast-Invariant Orientation Tuning in Simple Cells of Cat Visual Cortex , 2007, Neuron.