Estimating the influence of attention on population codes in human visual cortex using voxel-based tuning functions

In order to form stable perceptual representations, populations of sensory neurons must pool their output to overcome physiological noise; selective attention is then required to ensure that behaviorally relevant stimuli dominate these 'population codes' to gain access to awareness. However, the role that attention plays in shaping population response profiles has received little direct investigation, in part because most traditional neurophysiological methods cannot simultaneously assess changes in activity across large populations of sensory neurons. Based on single-unit recording studies, current theories hold that attending to a relevant feature sharpens the population response profile and improves the signal-to-noise ratio of the resulting perceptual representation. Here, we test this hypothesis using fMRI and an analysis approach that is able to estimate the influence of feature-based attentional modulations on population response profiles. We first derive orientation tuning functions for single voxels in human primary visual cortex, and then use these tuning functions to sort voxels according to their orientation preference. We then show that selective attention systematically biases population response profiles so that behaviorally relevant stimuli are represented in the visual system at the expense of behaviorally irrelevant stimuli. Collectively, the present results (1) provide a new approach for precisely characterizing feature-selective responses in human sensory cortices and (2) reveal how behavioral goals can shape population response profiles to support the formation of coherent perceptual representations.

[1]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[2]  Alexander Borst,et al.  Information theory and neural coding , 1999, Nature Neuroscience.

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

[4]  Jens Schwarzbach,et al.  Cerebral Cortex Advance Access published May 27, 2004 Control of Object-based Attention in Human Cortex , 2022 .

[5]  Wei Ji Ma,et al.  Bayesian inference with probabilistic population codes , 2006, Nature Neuroscience.

[6]  G. Boynton,et al.  Feature-Based Attentional Modulations in the Absence of Direct Visual Stimulation , 2007, Neuron.

[7]  G. Rees,et al.  Predicting the orientation of invisible stimuli from activity in human primary visual cortex , 2005, Nature Neuroscience.

[8]  Zhaoping Li,et al.  Psychophysical Tests of the Hypothesis of a Bottom-Up Saliency Map in Primary Visual Cortex , 2007, PLoS Comput. Biol..

[9]  C. Furmanski,et al.  An oblique effect in human primary visual cortex , 2000, Nature Neuroscience.

[10]  R. Zemel,et al.  Inference and computation with population codes. , 2003, Annual review of neuroscience.

[11]  J. Movshon,et al.  A computational analysis of the relationship between neuronal and behavioral responses to visual motion , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  Anthony J. Movshon,et al.  Optimal representation of sensory information by neural populations , 2006, Nature Neuroscience.

[13]  F. Campbell,et al.  The effect of orientation on the visual resolution of gratings , 1966, The Journal of physiology.

[14]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[15]  G. Orban,et al.  The organization of orientation selectivity throughout macaque visual cortex. , 2002, Cerebral cortex.

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

[17]  M. Mcmahon,et al.  The origin of the oblique effect examined with pattern adaptation and masking. , 2003, Journal of vision.

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

[19]  Stefan Treue,et al.  Different populations of neurons contribute to the detection and discrimination of visual motion , 2001, Vision Research.

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

[21]  J. Movshon,et al.  A new perceptual illusion reveals mechanisms of sensory decoding , 2007, Nature.

[22]  L. Itti,et al.  Search Goal Tunes Visual Features Optimally , 2007, Neuron.

[23]  Paul E. Downing,et al.  Using multi-voxel pattern analysis of fMRI data to interpret overlapping functional activations , 2007, Trends in Cognitive Sciences.

[24]  J. Gallant,et al.  Identifying natural images from human brain activity , 2008, Nature.

[25]  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.

[26]  D. Regan,et al.  Postadaptation orientation discrimination. , 1985, Journal of the Optical Society of America. A, Optics and image science.

[27]  Fuhui Long,et al.  Feature selection based on mutual information criteria of max-dependency, max-relevance, and min-redundancy , 2003, IEEE Transactions on Pattern Analysis and Machine Intelligence.

[28]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[29]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[30]  David D. Cox,et al.  Functional magnetic resonance imaging (fMRI) “brain reading”: detecting and classifying distributed patterns of fMRI activity in human visual cortex , 2003, NeuroImage.

[31]  Peter E. Latham,et al.  The relevance of Fisher Information for theories of cortical computation and attention , 2001 .

[32]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[33]  G. Orban,et al.  Human orientation discrimination tested with long stimuli , 1984, Vision Research.

[34]  D. Butts,et al.  Tuning Curves, Neuronal Variability, and Sensory Coding , 2006, PLoS biology.

[35]  Joel L. Davis,et al.  Visual attention and cortical circuits , 2001 .

[36]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[37]  Daniel Kahneman,et al.  Stroboscope motion: Effects of duration and interval1 , 1970 .

[38]  A P Georgopoulos,et al.  On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  G. Boynton Attention and visual perception , 2005, Current Opinion in Neurobiology.

[40]  Geoffrey M Boynton,et al.  The Representation of Behavioral Choice for Motion in Human Visual Cortex , 2007, The Journal of Neuroscience.

[41]  T. Sanger,et al.  Probability density estimation for the interpretation of neural population codes. , 1996, Journal of neurophysiology.

[42]  F. Tong,et al.  Decoding the visual and subjective contents of the human brain , 2005, Nature Neuroscience.

[43]  N. Kanwisher,et al.  Only some spatial patterns of fMRI response are read out in task performance , 2007, Nature Neuroscience.

[44]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[45]  Tsotsos Limited Capacity of Any Realizable Perceptual System Is a Sufficient Reason for Attentive Behavior , 1997, Consciousness and cognition.

[46]  Robert T. Knight,et al.  Spatio-temporal information analysis of event-related BOLD responses , 2007, NeuroImage.

[47]  F. Tong,et al.  Decoding Seen and Attended Motion Directions from Activity in the Human Visual Cortex , 2006, Current Biology.

[48]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

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

[50]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[51]  H Sompolinsky,et al.  Simple models for reading neuronal population codes. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[52]  M. Paradiso,et al.  A theory for the use of visual orientation information which exploits the columnar structure of striate cortex , 2004, Biological Cybernetics.

[53]  Daniel Yoshor,et al.  Spatial Attention Does Not Strongly Modulate Neuronal Responses in Early Human Visual Cortex , 2007, The Journal of Neuroscience.

[54]  B. Biswal,et al.  High‐resolution fMRI using multislice partial k‐space GR‐EPI with cubic voxels , 2001, Magnetic resonance in medicine.

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

[56]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

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