Choice-Related Activity during Visual Slant Discrimination in Macaque CIP But Not V3A

Abstract Creating three-dimensional (3D) representations of the world from two-dimensional retinal images is fundamental to visually guided behaviors including reaching and grasping. A critical component of this process is determining the 3D orientation of objects. Previous studies have shown that neurons in the caudal intraparietal area (CIP) of the macaque monkey represent 3D planar surface orientation (i.e., slant and tilt). Here we compare the responses of neurons in areas V3A (which is implicated in 3D visual processing and precedes CIP in the visual hierarchy) and CIP to 3D-oriented planar surfaces. We then examine whether activity in these areas correlates with perception during a fine slant discrimination task in which the monkeys report if the top of a surface is slanted toward or away from them. Although we find that V3A and CIP neurons show similar sensitivity to planar surface orientation, significant choice-related activity during the slant discrimination task is rare in V3A but prominent in CIP. These results implicate both V3A and CIP in the representation of 3D surface orientation, and suggest a functional dissociation between the areas based on slant-related choice signals.

[1]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[2]  W. Newsome,et al.  Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Ari Rosenberg,et al.  Reliability-dependent contributions of visual orientation cues in parietal cortex , 2014, Proceedings of the National Academy of Sciences.

[4]  John H R Maunsell,et al.  Potential confounds in estimating trial-to-trial correlations between neuronal response and behavior using choice probabilities. , 2012, Journal of neurophysiology.

[5]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[6]  Denis Schluppeck,et al.  7 Tesla fMRI Reveals Systematic Functional Organization for Binocular Disparity in Dorsal Visual Cortex , 2015, The Journal of Neuroscience.

[7]  Peter Janssen,et al.  Anterior Regions of Monkey Parietal Cortex Process Visual 3D Shape , 2007, Neuron.

[8]  B. Cumming,et al.  Decision-related activity in sensory neurons reflects more than a neuron’s causal effect , 2009, Nature.

[9]  Rufin Vogels,et al.  Convergence of Depth from Texture and Depth from Disparity in Macaque Inferior Temporal Cortex , 2004, The Journal of Neuroscience.

[10]  G. DeAngelis,et al.  Coding of Stereoscopic Depth Information in Visual Areas V3 and V3A , 2011, The Journal of Neuroscience.

[11]  Peter Janssen,et al.  Caudal Intraparietal Sulcus and three-dimensional vision: A combined functional magnetic resonance imaging and single-cell study , 2018, NeuroImage.

[12]  Takahisa M. Sanada,et al.  Representation of 3-D surface orientation by velocity and disparity gradient cues in area MT. , 2012, Journal of Neurophysiology.

[13]  A. Pouget,et al.  Information-limiting correlations , 2014, Nature Neuroscience.

[14]  Hiroshi Ban,et al.  fMRI Analysis-by-Synthesis Reveals a Dorsal Hierarchy That Extracts Surface Slant , 2015, The Journal of Neuroscience.

[15]  H. Sakata,et al.  Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. , 2000, Journal of neurophysiology.

[16]  K. H. Britten,et al.  A relationship between behavioral choice and the visual responses of neurons in macaque MT , 1996, Visual Neuroscience.

[17]  C. Connor,et al.  Three-dimensional orientation tuning in macaque area V4 , 2002, Nature Neuroscience.

[18]  Muge M. Bakircioglu,et al.  Mapping visual cortex in monkeys and humans using surface-based atlases , 2001, Vision Research.

[19]  Ari Rosenberg,et al.  The Visual Representation of 3D Object Orientation in Parietal Cortex , 2013, The Journal of Neuroscience.

[20]  G. DeAngelis,et al.  How Can Single Sensory Neurons Predict Behavior? , 2015, Neuron.

[21]  A. Parker,et al.  Quantitative analysis of the responses of V1 neurons to horizontal disparity in dynamic random-dot stereograms. , 2002, Journal of neurophysiology.

[22]  C L Colby,et al.  Visual, saccade-related, and cognitive activation of single neurons in monkey extrastriate area V3A. , 2000, Journal of neurophysiology.

[23]  Yong Gu,et al.  Evidence for a Causal Contribution of Macaque Vestibular, But Not Intraparietal, Cortex to Heading Perception , 2016, The Journal of Neuroscience.

[24]  H. Sakata,et al.  Integration of perspective and disparity cues in surface-orientation-selective neurons of area CIP. , 2001, Journal of neurophysiology.

[25]  James M. Hillis,et al.  Slant from texture and disparity cues: optimal cue combination. , 2004, Journal of vision.

[26]  Jerry D. Nguyenkim,et al.  Disparity-Based Coding of Three-Dimensional Surface Orientation by Macaque Middle Temporal Neurons , 2003, The Journal of Neuroscience.

[27]  Bruce G Cumming,et al.  Feedforward and Feedback Sources of Choice Probability in Neural Population Responses This Review Comes from a Themed Issue on Neurobiology of Cognitive Behavior Evidence for Feed-forward Models and Optimal Linear Readout? , 2022 .

[28]  H. Sakata,et al.  Parietal neurons represent surface orientation from the gradient of binocular disparity. , 2000, Journal of neurophysiology.

[29]  G. DeAngelis,et al.  Neural correlates of multisensory cue integration in macaque MSTd , 2008, Nature Neuroscience.

[30]  A. Parker,et al.  Perceptually Bistable Three-Dimensional Figures Evoke High Choice Probabilities in Cortical Area MT , 2001, The Journal of Neuroscience.

[31]  Ari Rosenberg,et al.  Gravity Influences the Visual Representation of Object Tilt in Parietal Cortex , 2014, The Journal of Neuroscience.

[32]  Dora E Angelaki,et al.  Functional Specializations of the Ventral Intraparietal Area for Multisensory Heading Discrimination , 2013, The Journal of Neuroscience.

[33]  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.

[34]  B. Cumming,et al.  Macaque V2 Neurons, But Not V1 Neurons, Show Choice-Related Activity , 2006, The Journal of Neuroscience.

[35]  S. Zeki.  Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. , 1978, The Journal of physiology.

[36]  G. DeAngelis,et al.  Decoupled choice-driven and stimulus-related activity in parietal neurons may be misrepresented by choice probabilities , 2017, Nature Communications.

[37]  C. Galletti,et al.  Gaze-dependent visual neurons in area V3A of monkey prestriate cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  S. Zeki,et al.  The third visual complex of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[39]  Hongdian Yang,et al.  Origins of choice-related activity in mouse somatosensory cortex , 2015, Nature Neuroscience.

[40]  S. Zeki.  Functional specialisation in the visual cortex of the rhesus monkey , 1978, Nature.

[41]  F A Wichmann,et al.  Ning for Helpful Comments and Suggestions. This Paper Benefited Con- Siderably from Conscientious Peer Review, and We Thank Our Reviewers the Psychometric Function: I. Fitting, Sampling, and Goodness of Fit , 2001 .

[42]  R. Vogels,et al.  Contribution of Inferior Temporal and Posterior Parietal Activity to Three-Dimensional Shape Perception , 2010, Current Biology.

[43]  M. Bethge,et al.  Inferring decoding strategies from choice probabilities in the presence of correlated variability , 2013, Nature Neuroscience.

[44]  S. E. Kwon,et al.  Sensory and decision-related activity propagate in a cortical feedback loop during touch perception , 2016, Nature Neuroscience.

[45]  H. Sakata,et al.  From Three-Dimensional Space Vision to Prehensile Hand Movements: The Lateral Intraparietal Area Links the Area V3A and the Anterior Intraparietal Area in Macaques , 2001, The Journal of Neuroscience.

[46]  Yong Gu,et al.  Causal Links between Dorsal Medial Superior Temporal Area Neurons and Multisensory Heading Perception , 2012, The Journal of Neuroscience.

[47]  Doris Y. Tsao,et al.  Stereopsis Activates V3A and Caudal Intraparietal Areas in Macaques and Humans , 2003, Neuron.

[48]  R. Andersen,et al.  Response of MSTd neurons to simulated 3D orientation of rotating planes. , 2002, Journal of neurophysiology.

[49]  Peter Janssen,et al.  Posterior Parietal Cortex Drives Inferotemporal Activations During Three-Dimensional Object Vision , 2016, PLoS biology.

[50]  R. Vogels,et al.  Inferotemporal Cortex Subserves Three-Dimensional Structure Categorization , 2012, Neuron.

[51]  Jonathan W. Pillow,et al.  Dissociated functional significance of decision-related activity in the primate dorsal stream , 2016, Nature.