Divisive Normalization Predicts Adaptation-Induced Response Changes in Macaque Inferior Temporal Cortex

Stimulus repetition alters neural responses to the repeated stimulus. This so-called adaptation phenomenon has been commonly observed at multiple spatial and temporal scales and in different brain areas, and has been hypothesized to affect the neural representation of the sensory input. Yet, the neural mechanisms underlying adaptation still remain unclear, especially in higher-order cortical areas. Here we employ a divisive normalization model of neural responses to predict adaptation-induced changes in responses of single neurons in the macaque inferior temporal (IT) cortex. According to this model, the response of a neuron is determined by an interplay between its direct excitatory and divisive normalizing inputs, with each input being subject to adaptation. To test the model, we recorded the responses of single IT cortex neurons to complex visual stimuli while separately adapting the two putative types of input to those neurons. We compared the changes in responses of these neurons following such adaptation with predictions derived from the divisive normalization model. As predicted by the model, we show that adaptation in the IT cortex can, depending on the relative strength of each putative type of input to a neuron, suppress or enhance the neural response to a complex stimulus. More generally, our data suggest that adaptation serves to selectively enhance processing of the stimuli that differ from recently experienced ones, even when these occur within a configuration of multiple stimuli. SIGNIFICANCE STATEMENT Stimulus repetition alters neural responses to the repeated stimulus. This so-called adaptation phenomenon has been robustly demonstrated in brains of different species and is considered to be a form of short-term plasticity inherent to the processing of sensory stimuli. Nevertheless, the functional role and underlying mechanisms of adaptation remain unclear. Here we demonstrate that divisive normalization, a canonical neural computation operating throughout the brain, predicts the adaptation-induced changes in response of single neurons to complex stimulus configurations in the macaque inferotemporal cortex. Our findings embed adaptation effects of inferotemporal neurons into the context of a broader neural network perspective that includes divisive normalization. Additionally, our findings have implications for understanding of the function of adaptation in higher-order sensory cortices.

[1]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[2]  Carson C. Chow,et al.  Competitive dynamics in cortical responses to visual stimuli. , 2005, Journal of neurophysiology.

[3]  S. Solomon,et al.  Moving Sensory Adaptation beyond Suppressive Effects in Single Neurons , 2014, Current Biology.

[4]  R. Klein,et al.  Modeling inhibition of return as short-term depression of early sensory input to the superior colliculus , 2011, Vision Research.

[5]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[6]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[7]  T. Sato,et al.  Interactions of visual stimuli in the receptive fields of inferior temporal neurons in awake macaques , 2004, Experimental Brain Research.

[8]  A. Kohn,et al.  Distinct Effects of Brief and Prolonged Adaptation on Orientation Tuning in Primary Visual Cortex , 2013, The Journal of Neuroscience.

[9]  R. Vogels,et al.  Properties of shape tuning of macaque inferior temporal neurons examined using rapid serial visual presentation. , 2007, Journal of neurophysiology.

[10]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Katsumi Watanabe,et al.  Inhibition of return in averaging saccades , 2001, Experimental Brain Research.

[12]  I. Biederman,et al.  Localizing the cortical region mediating visual awareness of object identity. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Matthew D. Hilchey,et al.  Returning to "inhibition of return" by dissociating long-term oculomotor IOR from short-term sensory adaptation and other nonoculomotor "inhibitory" cueing effects. , 2014, Journal of experimental psychology. Human perception and performance.

[14]  R. Desimone,et al.  Spectral properties of V4 neurons in the macaque , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[16]  Adam Kohn,et al.  The influence of surround suppression on adaptation effects in primary visual cortex. , 2012, Journal of neurophysiology.

[17]  Amy M. Ni,et al.  Tuned Normalization Explains the Size of Attention Modulations , 2012, Neuron.

[18]  G. Orban,et al.  Shape interactions in macaque inferior temporal neurons. , 1999, Journal of neurophysiology.

[19]  R. Vogels,et al.  Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. , 2010, Cerebral cortex.

[20]  R. Desimone,et al.  Inferior temporal mechanisms for invariant object recognition. , 1994, Cerebral cortex.

[21]  D. Sagi,et al.  Tilt aftereffect due to adaptation to natural stimuli , 2015, Vision Research.

[22]  What causes IOR? Attention or perception? – Manipulating cue and target luminance in either blocked or mixed condition , 2014, Vision Research.

[23]  P. Lennie,et al.  Multiple Adaptable Mechanisms Early in the Primate Visual Pathway , 2011, The Journal of Neuroscience.

[24]  Rufin Vogels,et al.  Stimulus repetition probability does not affect repetition suppression in macaque inferior temporal cortex. , 2011, Cerebral cortex.

[25]  M. Posner,et al.  Components of visual orienting , 1984 .

[26]  Yan Liu,et al.  Time course and stimulus dependence of repetition-induced response suppression in inferotemporal cortex. , 2009, Journal of neurophysiology.

[27]  R. Wurtz,et al.  Visual responses of inferior temporal neurons in awake rhesus monkey. , 1983, Journal of neurophysiology.

[28]  M. Tovée,et al.  The responses of single neurons in the temporal visual cortical areas of the macaque when more than one stimulus is present in the receptive field , 2004, Experimental Brain Research.

[29]  David H. Do,et al.  Dissociable Perceptual Effects of Visual Adaptation , 2009, PloS one.

[30]  Hossein Esteky,et al.  Neuronal Correlates of View Representation Revealed by Face-View Aftereffect , 2013, The Journal of Neuroscience.

[31]  I. Fujita,et al.  Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex , 2000, Nature Neuroscience.

[32]  Rufin Vogels,et al.  Effect of Adaptation on Object Representation Accuracy in Macaque Inferior Temporal Cortex , 2013, Journal of Cognitive Neuroscience.

[33]  E. Miller,et al.  Suppression of visual responses of neurons in inferior temporal cortex of the awake macaque by addition of a second stimulus , 1993, Brain Research.

[34]  R. Vogels,et al.  Neurons in Macaque Inferior Temporal Cortex Show No Surprise Response to Deviants in Visual Oddball Sequences , 2014, The Journal of Neuroscience.

[35]  R. Vogels,et al.  Spatial sensitivity of macaque inferior temporal neurons , 2000, The Journal of comparative neurology.

[36]  James J DiCarlo,et al.  Multiple Object Response Normalization in Monkey Inferotemporal Cortex , 2005, The Journal of Neuroscience.

[37]  Rafael Malach,et al.  Targeting the functional properties of cortical neurons using fMR-adaptation , 2012, NeuroImage.

[38]  G. Rhodes,et al.  Repetition Suppression in Ventral Visual Cortex Is Diminished as a Function of Increasing Autistic Traits , 2014, Cerebral cortex.

[39]  S. Morad,et al.  Ceramide-orchestrated signalling in cancer cells , 2012, Nature Reviews Cancer.

[40]  G. Orban,et al.  Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm , 2006, Neuron.

[41]  M. Carandini,et al.  Normalization as a canonical neural computation , 2011, Nature Reviews Neuroscience.

[42]  G. Orban,et al.  How task-related are the responses of inferior temporal neurons? , 1995, Visual Neuroscience.

[43]  G. DeAngelis,et al.  A Normalization Model of Multisensory Integration , 2011, Nature Neuroscience.

[44]  M. Webster,et al.  Visual adaptation: Neural, psychological and computational aspects , 2007, Vision Research.

[45]  Saumil S. Patel,et al.  Shape effects on reflexive spatial selective attention and a plausible neurophysiological model , 2010, Vision Research.

[46]  C. Olson,et al.  Repetition suppression in monkey inferotemporal cortex: relation to behavioral priming. , 2007, Journal of neurophysiology.

[47]  R. Desimone,et al.  Responses of Neurons in Inferior Temporal Cortex during Memory- Guided Visual Search , 1998 .

[48]  Rufin Vogels,et al.  Stimulus repetition affects both strength and synchrony of macaque inferior temporal cortical activity. , 2012, Journal of neurophysiology.