Supralinear and Supramodal Integration of Visual and Tactile Signals in Rats: Psychophysics and Neuronal Mechanisms

Summary To better understand how object recognition can be triggered independently of the sensory channel through which information is acquired, we devised a task in which rats judged the orientation of a raised, black and white grating. They learned to recognize two categories of orientation: 0° ± 45° (“horizontal”) and 90° ± 45° (“vertical”). Each trial required a visual (V), a tactile (T), or a visual-tactile (VT) discrimination; VT performance was better than that predicted by optimal linear combination of V and T signals, indicating synergy between sensory channels. We examined posterior parietal cortex (PPC) and uncovered key neuronal correlates of the behavioral findings: PPC carried both graded information about object orientation and categorical information about the rat’s upcoming choice; single neurons exhibited identical responses under the three modality conditions. Finally, a linear classifier of neuronal population firing replicated the behavioral findings. Taken together, these findings suggest that PPC is involved in the supramodal processing of shape.

[1]  Giuliano Iurilli,et al.  Cellular and Synaptic Architecture of Multisensory Integration in the Mouse Neocortex , 2013, Neuron.

[2]  A. Wing,et al.  Active touch sensing , 2011, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  M. Brecht,et al.  Functional architecture of the mystacial vibrissae , 1997, Behavioural Brain Research.

[4]  Christoph Kayser,et al.  Asymmetric Multisensory Interactions of Visual and Somatosensory Responses in a Region of the Rat Parietal Cortex , 2013, PloS one.

[5]  R. Quian Quiroga,et al.  Unsupervised Spike Detection and Sorting with Wavelets and Superparamagnetic Clustering , 2004, Neural Computation.

[6]  D. Zoccolan,et al.  Transformation-Tolerant Object Recognition in Rats Revealed by Visual Priming , 2012, The Journal of Neuroscience.

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

[8]  Olaf Sporns,et al.  Network Analysis of Corticocortical Connections Reveals Ventral and Dorsal Processing Streams in Mouse Visual Cortex , 2012, The Journal of Neuroscience.

[9]  Giuliano Iurilli,et al.  Sound-Driven Synaptic Inhibition in Primary Visual Cortex , 2012, Neuron.

[10]  Alexandre Pouget,et al.  Tuning the speed-accuracy trade-off to maximize reward rate in multisensory decision-making , 2015, eLife.

[11]  D. Zoccolan.  Invariant visual object recognition and shape processing in rats , 2015, Behavioural Brain Research.

[12]  Rune W. Berg,et al.  Rhythmic whisking by rat: retraction as well as protraction of the vibrissae is under active muscular control. , 2003, Journal of neurophysiology.

[13]  R. Jacobs,et al.  Optimal integration of texture and motion cues to depth , 1999, Vision Research.

[14]  R. L. Reep,et al.  Rat posterior parietal cortex: topography of corticocortical and thalamic connections , 2004, Experimental Brain Research.

[15]  B. J. Clark,et al.  Cortical connectivity maps reveal anatomically distinct areas in the parietal cortex of the rat , 2015, Front. Neural Circuits.

[16]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[17]  Christopher R Fetsch,et al.  Dynamic Reweighting of Visual and Vestibular Cues during Self-Motion Perception , 2009, The Journal of Neuroscience.

[18]  David Raposo,et al.  Multisensory Decision-Making in Rats and Humans , 2012, The Journal of Neuroscience.

[19]  L. Krubitzer.  The organization of neocortex in mammals: are species differences really so different? , 1995, Trends in Neurosciences.

[20]  David S. Greenberg,et al.  Rats maintain an overhead binocular field at the expense of constant fusion , 2013, Nature.

[21]  David G. Stork,et al.  Pattern Classification , 1973 .

[22]  B. Kolb,et al.  Behavioural and anatomical studies of the posterior parietal cortex in the rat , 1987, Behavioural Brain Research.

[23]  J. H. Jamison.  Measurement of auditory intensity thresholds in the rat by conditioning of an autonomic response. , 1951, Journal of comparative and physiological psychology.

[24]  I. Whishaw,et al.  Variation in visual acuity within pigmented, and between pigmented and albino rat strains , 2002, Behavioural Brain Research.

[25]  M. Diamond,et al.  Behavioral study of whisker-mediated vibration sensation in rats , 2012, Proceedings of the National Academy of Sciences.

[26]  Matthew T. Kaufman,et al.  Posterior Parietal Cortex Guides Visual Decisions in Rats , 2016, The Journal of Neuroscience.

[27]  G. Leichnetz.  Connections of the medial posterior parietal cortex (area 7m) in the monkey , 2001, The Anatomical record.

[28]  I. T. Diamond,et al.  Chapter 18 – HEARING: CENTRAL NEURAL MECHANISMS , 1973 .

[29]  Roozbeh Kiani,et al.  Integration of Direction Cues Is Invariant to the Temporal Gap between Them , 2013, The Journal of Neuroscience.

[30]  Nikos K Logothetis,et al.  A toolbox for the fast information analysis of multiple-site LFP, EEG and spike train recordings , 2009, BMC Neuroscience.

[31]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[32]  G. Gourevitch,et al.  Audibility in the rat. , 1966, Journal of comparative and physiological psychology.

[33]  Matthew T. Kaufman,et al.  A category-free neural population supports evolving demands during decision-making , 2014, Nature Neuroscience.

[34]  Zengcai V. Guo,et al.  Flow of Cortical Activity Underlying a Tactile Decision in Mice , 2014, Neuron.

[35]  Konrad Paul Kording,et al.  Review TRENDS in Cognitive Sciences Vol.10 No.7 July 2006 Special Issue: Probabilistic models of cognition Bayesian decision theory in sensorimotor control , 2022 .

[36]  Bingni W. Brunton,et al.  Distinct effects of prefrontal and parietal cortex inactivations on an accumulation of evidence task in the rat , 2015, bioRxiv.

[37]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[38]  Robert A Jacobs,et al.  Bayesian integration of visual and auditory signals for spatial localization. , 2003, Journal of the Optical Society of America. A, Optics, image science, and vision.

[39]  H. Killackey,et al.  Organization of corticocortical connections in the parietal cortex of the rat , 1978, The Journal of comparative neurology.

[40]  Christopher R Fetsch,et al.  Neural correlates of reliability-based cue weighting during multisensory integration , 2011, Nature Neuroscience.

[41]  C. Koch,et al.  Invariant visual representation by single neurons in the human brain , 2005, Nature.

[42]  Jonathan R. Whitlock,et al.  Navigating from hippocampus to parietal cortex , 2008, Proceedings of the National Academy of Sciences.

[43]  Wojtek J. Krzanowski,et al.  Principles of multivariate analysis : a user's perspective. oxford , 1988 .

[44]  M. Quirk,et al.  Representation of Spatial Goals in Rat Orbitofrontal Cortex , 2006, Neuron.

[45]  Justus Liebig,et al.  Progress in Sensory Physiology , 1981, Progress in Sensory Physiology.

[46]  Brian Zingg,et al.  Cross-Modality Sharpening of Visual Cortical Processing through Layer-1-Mediated Inhibition and Disinhibition , 2016, Neuron.

[47]  Henry E. Heffner,et al.  Audiogram of the hooded Norway rat , 1994, Hearing Research.

[48]  G. M. Martin,et al.  A Role for Olfaction in Object Recognition by Normal and Hippocampal-Damaged Rats , 2002, Neurobiology of Learning and Memory.

[49]  Timothy D. Hanks,et al.  Bounded Integration in Parietal Cortex Underlies Decisions Even When Viewing Duration Is Dictated by the Environment , 2008, The Journal of Neuroscience.

[50]  D. Burr,et al.  The Ventriloquist Effect Results from Near-Optimal Bimodal Integration , 2004, Current Biology.

[51]  R. Frostig,et al.  Whisker-based discrimination of object orientation determined with a rapid training paradigm , 2005, Neurobiology of Learning and Memory.

[52]  D. G. Green,et al.  Single retinal ganglion cell responses in the dark-reared rat: Grating acuity, contrast sensitivity, and defocusing , 1978, Vision Research.

[53]  G. Gourevitch.  AUDITORY MASKING IN THE RAT. , 1965, Journal of the Acoustical Society of America.

[54]  Christopher D. Harvey,et al.  Choice-specific sequences in parietal cortex during a virtual-navigation decision task , 2012, Nature.

[55]  Bence P Ölveczky,et al.  Motoring ahead with rodents , 2011, Current Opinion in Neurobiology.

[56]  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 .

[57]  Diana K. Sarko,et al.  Convergent approaches toward the study of multisensory perception , 2013, Front. Syst. Neurosci..

[58]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[59]  B. Vogt,et al.  Direct connections of rat visual cortex with sensory, motor, and association cortices , 1984, The Journal of comparative neurology.

[60]  Alexandre Pouget,et al.  Optimal multisensory decision-making in a reaction-time task , 2014, eLife.

[61]  L. A. Pennington,et al.  An Improved Conditioning Technique for Determining Auditory Acuity of the Rat , 1943 .

[62]  Houman Safaai,et al.  Coordinated Population Activity Underlying Texture Discrimination in Rat Barrel Cortex , 2013, The Journal of Neuroscience.

[63]  M. Landy,et al.  Ideal-Observer Models of Cue Integration , 2012 .

[64]  J. Kelly,et al.  Auditory sensitivity of the albino rat. , 1976, Journal of comparative and physiological psychology.

[65]  Gregory C. DeAngelis,et al.  Bridging the gap between theories of sensory cue integration and the physiology of multisensory neurons , 2013, Nature Reviews Neuroscience.