Distracter suppression dominates attentional modulation of responses to multiple stimuli inside the receptive fields of middle temporal neurons

Single‐cell studies in macaques have shown that attending to one of two stimuli, positioned inside a visual neuron's receptive field (RF), modulates the neuron's response to reflect the features of the attended stimulus. Such a modulation has been described as a ‘push–pull’ effect relative to a reference response: a neuron's response increases when attention is directed to a preferred stimulus, and decreases when attention is directed to a non‐preferred stimulus. It has been further suggested that the response increase when attending to a preferred stimulus is the predominant effect. Here, we show that the observed attentional modulation depends on the reference response. We recorded neuronal responses in motion processing area middle temporal (MT) of macaques to two moving random dot patterns positioned inside neurons’ RF. One pattern always moved in the neuron's antipreferred direction (null pattern), while the other moved in one of 12 directions (tuning pattern). At the beginning of a trial, a cue indicated the location and direction of the target. The animal was required to release a lever when a change in the target direction occurred, and to ignore changes in the distracter. Relative to neurons’ initial responses to the dual stimuli (when attention was less likely to modulate responses), attending to the tuning pattern did not significantly modulate responses over time. However, attending to the null pattern progressively decreased responses over time. These results were quantitatively described by filter and input gain models, characterising a predominant response suppression relative to a reference response, rather than response enhancement.

[1]  Nicholas A. Steinmetz,et al.  Top-down control of visual attention , 2010, Current Opinion in Neurobiology.

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

[3]  R A Andersen,et al.  The response of area MT and V1 neurons to transparent motion , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

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

[6]  J. Maunsell,et al.  The role of attention in visual processing. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[7]  E. Seidemann,et al.  Effect of spatial attention on the responses of area MT neurons. , 1999, Journal of neurophysiology.

[8]  R. Duncan Luce,et al.  Response Times: Their Role in Inferring Elementary Mental Organization , 1986 .

[9]  R. Wurtz,et al.  Responses of MT and MST neurons to one and two moving objects in the receptive field. , 1997, Journal of neurophysiology.

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

[11]  K. H. Britten,et al.  Spatial Summation in the Receptive Fields of MT Neurons , 1999, The Journal of Neuroscience.

[12]  John H. R. Maunsell,et al.  Attentional modulation of visual motion processing in cortical areas MT and MST , 1996, Nature.

[13]  Carrie J. McAdams,et al.  Effects of Attention on the Reliability of Individual Neurons in Monkey Visual Cortex , 1999, Neuron.

[14]  Stefan Treue,et al.  Multifocal Attention Filters Targets from Distracters within and beyond Primate MT Neurons' Receptive Field Boundaries , 2011, Neuron.

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

[16]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[17]  Geoffrey M. Ghose,et al.  Attentional modulation in visual cortex depends on task timing , 2002, Nature.

[18]  J. Maunsell,et al.  Spatial Summation Can Explain the Attentional Modulation of Neuronal Responses to Multiple Stimuli in Area V4 , 2008, The Journal of Neuroscience.

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

[20]  John H. R. Maunsell,et al.  Attention to both space and feature modulates neuronal responses in macaque area V4. , 2000, Journal of neurophysiology.

[21]  Guillaume A. Rousselet,et al.  Robust Correlation Analyses: False Positive and Power Validation Using a New Open Source Matlab Toolbox , 2012, Front. Psychology.

[22]  Paul S Khayat,et al.  Attention Differentially Modulates Similar Neuronal Responses Evoked by Varying Contrast and Direction Stimuli in Area MT , 2010, The Journal of Neuroscience.

[23]  H. Akaike,et al.  Information Theory and an Extension of the Maximum Likelihood Principle , 1973 .

[24]  Eero P. Simoncelli,et al.  A model of neuronal responses in visual area MT , 1998, Vision Research.

[25]  G. Boynton A framework for describing the effects of attention on visual responses , 2009, Vision Research.

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

[27]  J. Martinez-Trujillo,et al.  Effects of attention and distractor contrast on the responses of middle temporal area neurons to transient motion direction changes , 2015, The European journal of neuroscience.

[28]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.