Not Just for Bimodal Neurons Anymore: The Contribution of Unimodal Neurons to Cortical Multisensory Processing

Traditionally, neuronal studies of multisensory processing proceeded by first identifying neurons that were overtly multisensory (e.g., bimodal, trimodal) and then testing them. In contrast, the present study examined, without precondition, neurons in an extrastriate visual area of the cat for their responses to separate (visual, auditory) and combined-modality (visual and auditory) stimulation. As expected, traditional bimodal forms of multisensory neurons were identified. In addition, however, many neurons that were activated only by visual stimulation (i.e., unimodal) had that response modulated by the presence of an auditory stimulus. Some unimodal neurons showed multisensory responses that were statistically different from their visual response. Other unimodal neurons had subtle multisensory effects that were detectable only at the population level. Most surprisingly, these non-bimodal neurons generated more than twice the multisensory signal in the PLLS than did the bimodal neurons. These results expand the range of multisensory convergence patterns beyond that of the bimodal neuron. However, rather than characterize a separate class of multisensory neurons, unimodal multisensory neurons may actually represent an intermediary form of multisensory convergence that exists along the functional continuum between unisensory neurons, at one end, and fully bimodal neurons at the other.

[1]  R. Hill,et al.  Responsiveness to sensory stimulation of units in the superior colliculus and subjacent tectotegmental regions of the rabbit. , 1966, Experimental neurology.

[2]  I. Nelken,et al.  Physiological and Anatomical Evidence for Multisensory Interactions in Auditory Cortex , 2006, Cerebral cortex.

[3]  Brian L Allman,et al.  Multisensory processing in "unimodal" neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex. , 2007, Journal of neurophysiology.

[4]  E. Newman,et al.  Integration of visual and infrared information in bimodal neurons in the rattlesnake optic tectum. , 1981, Science.

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

[6]  M. Wallace,et al.  Integration of multiple sensory modalities in cat cortex , 2004, Experimental Brain Research.

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

[8]  B. Stein,et al.  Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration. , 1986, Journal of neurophysiology.

[9]  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.

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

[11]  H. R. Clemo,et al.  Sensory and multisensory representations within the cat rostral suprasylvian cortex , 2007, The Journal of comparative neurology.

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

[13]  B. Allman,et al.  Auditory projections to extrastriate visual cortex: connectional basis for multisensory processing in ‘unimodal’ visual neurons , 2008, Experimental Brain Research.

[14]  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.

[15]  Brian L Allman,et al.  Do cross-modal projections always result in multisensory integration? , 2008, Cerebral cortex.

[16]  Chris I. Baker,et al.  Integration of Visual and Auditory Information by Superior Temporal Sulcus Neurons Responsive to the Sight of Actions , 2005, Journal of Cognitive Neuroscience.

[17]  M. Alex Meredith,et al.  Crossmodal projections from somatosensory area SIV to the auditory field of the anterior ectosylvian sulcus (FAES) in Cat: further evidence for subthreshold forms of multisensory processing , 2006, Experimental Brain Research.

[18]  Leslie P. Keniston,et al.  Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: Sensory-specific versus non-specific coding , 2008, Brain Research.

[19]  Barry E Stein,et al.  Visual deprivation alters the development of cortical multisensory integration. , 2007, Journal of neurophysiology.

[20]  L. Palmer,et al.  The retinotopic organization of lateral suprasylvian visual areas in the cat , 1978, The Journal of comparative neurology.

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