Asymmetric Multisensory Interactions of Visual and Somatosensory Responses in a Region of the Rat Parietal Cortex

Perception greatly benefits from integrating multiple sensory cues into a unified percept. To study the neural mechanisms of sensory integration, model systems are required that allow the simultaneous assessment of activity and the use of techniques to affect individual neural processes in behaving animals. While rodents qualify for these requirements, little is known about multisensory integration and areas involved for this purpose in the rodent. Using optical imaging combined with laminar electrophysiological recordings, the rat parietal cortex was identified as an area where visual and somatosensory inputs converge and interact. Our results reveal similar response patterns to visual and somatosensory stimuli at the level of current source density (CSD) responses and multi-unit responses within a strip in parietal cortex. Surprisingly, a selective asymmetry was observed in multisensory interactions: when the somatosensory response preceded the visual response, supra-linear summation of CSD was observed, but the reverse stimulus order resulted in sub-linear effects in the CSD. This asymmetry was not present in multi-unit activity however, which showed consistently sub-linear interactions. These interactions were restricted to a specific temporal window, and pharmacological tests revealed significant local intra-cortical contributions to this phenomenon. Our results highlight the rodent parietal cortex as a system to model the neural underpinnings of multisensory processing in behaving animals and at the cellular level.

[1]  R. Frostig,et al.  Large-Scale Organization of Rat Sensorimotor Cortex Based on a Motif of Large Activation Spreads , 2008, The Journal of Neuroscience.

[2]  Elizabeth A. Clement,et al.  Cyclic and Sleep-Like Spontaneous Alternations of Brain State Under Urethane Anaesthesia , 2008, PloS one.

[3]  Jane Stewart,et al.  A descriptive study of social development in the rat (Rattus norvegicus) , 1981, Animal Behaviour.

[4]  D. Angelaki,et al.  Multisensory integration: resolving sensory ambiguities to build novel representations , 2010, Current Opinion in Neurobiology.

[5]  Paul J. Laurienti,et al.  On the use of superadditivity as a metric for characterizing multisensory integration in functional neuroimaging studies , 2005, Experimental Brain Research.

[6]  Christoph Kayser,et al.  Audio-Visual Detection Benefits in the Rat , 2012, PloS one.

[7]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[8]  T. Stanford,et al.  Superadditivity in multisensory integration: putting the computation in context. , 2007, Neuroreport.

[9]  B. Cragg The fate of axon terminals in visual cortex during trans-synaptic atrophy of the lateral geniculate nucleus. , 1971, Brain research.

[10]  O. Fehér,et al.  Sensory interactive zones in the rat cerebral cortex , 1986, Neuroscience.

[11]  Arthur W. Toga,et al.  Functional Signal- and Paradigm-Dependent Linear Relationships between Synaptic Activity and Hemodynamic Responses in Rat Somatosensory Cortex , 2004, The Journal of Neuroscience.

[12]  Christoph Kayser,et al.  Do early sensory cortices integrate cross-modal information? , 2007, Brain Structure and Function.

[13]  K. Harris,et al.  Laminar Structure of Spontaneous and Sensory-Evoked Population Activity in Auditory Cortex , 2009, Neuron.

[14]  D. Contreras,et al.  Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex , 2005, Nature Neuroscience.

[15]  F. Haiss,et al.  Spatiotemporal Dynamics of Cortical Sensorimotor Integration in Behaving Mice , 2007, Neuron.

[16]  Anthony M Zador,et al.  Millisecond-scale differences in neural activity in auditory cortex can drive decisions , 2008, Nature Neuroscience.

[17]  Laurie D. Burns,et al.  High-speed, miniaturized fluorescence microscopy in freely moving mice , 2008, Nature Methods.

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

[19]  Sidney S. Simon,et al.  Merging of the Senses , 2008, Front. Neurosci..

[20]  Jennifer K. Bizley,et al.  Visual influences on ferret auditory cortex , 2009, Hearing Research.

[21]  Yong Gu,et al.  Perceptual Learning Reduces Interneuronal Correlations in Macaque Visual Cortex , 2011, Neuron.

[22]  F. Ohl,et al.  Alteration of Auditory Cortex Activity with a Visual Stimulus through Conditioning: A 2-Deoxyglucose Analysis , 1996, Neurobiology of Learning and Memory.

[23]  Stefano Panzeri,et al.  Visual Enhancement of the Information Representation in Auditory Cortex , 2010, Current Biology.

[24]  L. Swanson The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[25]  C. Spence Explaining the Colavita visual dominance effect. , 2009, Progress in brain research.

[26]  Michael T. Lippert,et al.  Improvement of visual contrast detection by a simultaneous sound , 2007, Brain Research.

[27]  Kentaroh Takagaki,et al.  Crossmodal propagation of sensory-evoked and spontaneous activity in the rat neocortex , 2008, Neuroscience Letters.

[28]  Rogelio Luna,et al.  Do Sensory Cortices Process More than One Sensory Modality during Perceptual Judgments? , 2010, Neuron.

[29]  Atsushi Miyawaki,et al.  Lighting up cells: labelling proteins with fluorophores. , 2003, Nature cell biology.

[30]  D. Barth,et al.  Multisensory and secondary somatosensory cortex in the rat. , 2005, Cerebral cortex.

[31]  H Scheich,et al.  Functional organization of auditory cortex in the Mongolian gerbil (Meriones unguiculatus). III. Anatomical subdivisions and corticocortical connections , 2000, The European journal of neuroscience.

[32]  M. Sarter,et al.  Neuronal correlates of signal detection in the posterior parietal cortex of rats performing a sustained attention task , 2006, Neuroscience.

[33]  Bruno B Averbeck,et al.  Integration of Auditory and Visual Communication Information in the Primate Ventrolateral Prefrontal Cortex , 2006, The Journal of Neuroscience.

[34]  T. Stanford,et al.  Multisensory integration: current issues from the perspective of the single neuron , 2008, Nature Reviews Neuroscience.

[35]  A. Pouget,et al.  Reference frames for representing visual and tactile locations in parietal cortex , 2005, Nature Neuroscience.

[36]  Brian L Allman,et al.  Multisensory and unisensory neurons in ferret parietal cortex exhibit distinct functional properties , 2013, The European journal of neuroscience.

[37]  O. Blanke Multisensory brain mechanisms of bodily self-consciousness , 2012, Nature Reviews Neuroscience.

[38]  Brigitte Röder,et al.  Semantic confusion regarding the development of multisensory integration: a practical solution , 2010, The European journal of neuroscience.

[39]  A. Foust,et al.  State-dependent auditory evoked hemodynamic responses recorded optically with indwelling photodiodes. , 2009, Applied optics.

[40]  Yevgeniy B. Sirotin,et al.  Spatiotemporal precision and hemodynamic mechanism of optical point spreads in alert primates , 2009, Proceedings of the National Academy of Sciences.

[41]  M. Wallace,et al.  A revised view of sensory cortical parcellation , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[42]  S. Nishida,et al.  Recalibration of audiovisual simultaneity , 2004, Nature Neuroscience.

[43]  R. C. Tees The effects of posterior parietal and posterior temporal cortical lesions on multimodal spatial and nonspatial competencies in rats , 1999, Behavioural Brain Research.

[44]  B. Stein,et al.  Interactions among converging sensory inputs in the superior colliculus. , 1983, Science.

[45]  G. Calvert Crossmodal processing in the human brain: insights from functional neuroimaging studies. , 2001, Cerebral cortex.

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

[47]  T. Powell,et al.  An experimental study of the termination of the lateral geniculo–cortical pathway in the cat and monkey , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[48]  C. Nicholson,et al.  Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. , 1975, Journal of neurophysiology.

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

[50]  Brian L Allman,et al.  Subthreshold multisensory processing in cat auditory cortex , 2009, Neuroreport.

[51]  R. Douglas,et al.  Recurrent neuronal circuits in the neocortex , 2007, Current Biology.

[52]  U. Noppeney,et al.  Audiovisual Synchrony Improves Motion Discrimination via Enhanced Connectivity between Early Visual and Auditory Areas , 2010, The Journal of Neuroscience.

[53]  John J. Foxe,et al.  The case for feedforward multisensory convergence during early cortical processing , 2005, Neuroreport.

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

[55]  Holger Schulze,et al.  Auditory Cortical Contrast Enhancing by Global Winner-Take-All Inhibitory Interactions , 2008, PloS one.

[56]  O. Blanke,et al.  Multisensory Mechanisms in Temporo-Parietal Cortex Support Self-Location and First-Person Perspective , 2011, Neuron.

[57]  H. R. Clemo,et al.  Laminar and connectional organization of a multisensory cortex , 2013, The Journal of comparative neurology.

[58]  J. Pratte,et al.  Simultaneous assessment of rodent behavior and neurochemistry using a miniature positron emission tomograph , 2011, Nature Methods.

[59]  R. J. McDonald,et al.  Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. , 1994, Cerebral cortex.

[60]  T. Teyler,et al.  Laminar pattern of synaptic activity in rat primary visual cortex: comparison of in vivo and in vitro studies employing the current source density analysis , 1994, Brain Research.

[61]  B. Stein,et al.  Spatial determinants of multisensory integration in cat superior colliculus neurons. , 1996, Journal of neurophysiology.

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

[63]  Max F. K. Happel,et al.  Spectral Integration in Primary Auditory Cortex Attributable to Temporally Precise Convergence of Thalamocortical and Intracortical Input , 2010, The Journal of Neuroscience.

[64]  J. Olavarria,et al.  Rats with lesions in anteromedial extrastriate cortex fail to learn a visuosomatic conditional response , 1987, Behavioural Brain Research.

[65]  I. Whishaw,et al.  The Behavior of the Laboratory Rat , 2004 .

[66]  Jian-Young Wu,et al.  Compression and Reflection of Visually Evoked Cortical Waves , 2007, Neuron.

[67]  J. Driver,et al.  Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments , 2008, Neuron.

[68]  S. Panzeri,et al.  Role of precise spike timing in coding of dynamic vibrissa stimuli in somatosensory thalamus. , 2007, Journal of neurophysiology.

[69]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[70]  I. Q. Wishaw,et al.  THE BEHAVIOR OF THE LABORATORY RAT A Handbook with Tests , 2004 .

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

[72]  R. Kuzniecky,et al.  Autoradiographic evidence for the transmeningeal diffusion of muscimol into the neocortex in rats , 2012, Brain Research.

[73]  T Hori,et al.  Presynaptic inhibition by muscimol through GABAB receptors , 2000, The European journal of neuroscience.

[74]  Gidon Felsen,et al.  Neural Substrates of Sensory-Guided Locomotor Decisions in the Rat Superior Colliculus , 2008, Neuron.

[75]  Christoph Kayser,et al.  Spatial Organization of Multisensory Responses in Temporal Association Cortex , 2009, The Journal of Neuroscience.

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

[77]  C. E. Schroeder,et al.  Contribution of extrastriate area V4 to the surface-recorded flash VEP in the awake macaque , 1994, Vision Research.

[78]  N. Logothetis,et al.  Visual modulation of neurons in auditory cortex. , 2008, Cerebral cortex.

[79]  Christoph Kayser,et al.  Coupling of neural activity and fMRI-BOLD in the motion area MT. , 2010, Magnetic resonance imaging.

[80]  T. Stanford,et al.  Challenges in quantifying multisensory integration: alternative criteria, models, and inverse effectiveness , 2009, Experimental Brain Research.

[81]  J. Duhamel,et al.  Multisensory Integration in the Ventral Intraparietal Area of the Macaque Monkey , 2007, The Journal of Neuroscience.

[82]  Y. Sakurai,et al.  Functional role of the secondary visual cortex in multisensory facilitation in rats , 2008, Neuroscience.

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

[84]  Tony Ro,et al.  TMS of posterior parietal cortex disrupts visual tactile multisensory integration , 2010, The European journal of neuroscience.

[85]  Jeffery A Winer,et al.  A multisensory zone in rat parietotemporal cortex: Intra‐ and extracellular physiology and thalamocortical connections , 2003, The Journal of comparative neurology.

[86]  Boyer D Winters,et al.  A Distributed Cortical Representation Underlies Crossmodal Object Recognition in Rats , 2010, The Journal of Neuroscience.

[87]  B. Argall,et al.  Unraveling multisensory integration: patchy organization within human STS multisensory cortex , 2004, Nature Neuroscience.

[88]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[89]  Gonzalo H. Otazu,et al.  Engaging in an auditory task suppresses responses in auditory cortex , 2009, Nature Neuroscience.

[90]  David S. Greenberg,et al.  Population imaging of ongoing neuronal activity in the visual cortex of awake rats , 2008, Nature Neuroscience.

[91]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[92]  H. R. Clemo,et al.  Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence. , 2004, Cerebral cortex.

[93]  F. Colavita Human sensory dominance , 1974 .