Subthreshold auditory inputs to extrastriate visual neurons are responsive to parametric changes in stimulus quality: Sensory-specific versus non-specific coding

A new subthreshold form of multisensory processing has been recently identified that results from the convergence of suprathreshold excitatory inputs from one modality with subthreshold inputs from another. Because of the subthreshold nature of the second modality, descriptive measures of sensory features such as receptive field properties or location are not directly apparent as they are for traditional bimodal neurons. This raises the question of whether or not subthreshold signals actually convey sensory-specific receptive field information as seen in their bimodal counterparts, or if they represent non-specific effects such as arousal. The present experiment addressed this issue in visually-responsive neurons from the cat posterolateral lateral suprasylvian cortex (PLLS). Single-unit electrophysiological techniques were used to record neuronal responses to visual, auditory and combined visual-auditory stimuli while the intensity of stimulation in the subthreshold auditory modality was systematically altered. The results showed that subthreshold multisensory neurons were sensitive to changes in auditory stimulus intensity. These receptive field sensitivities are similar to those observed in bimodal neurons and thereby represent sensory-specific, not arousal-related responses. In addition, these results provide further support for the notion that multisensory processing occurs along a dynamic continuum of neuronal convergence patterns from bimodal to purely sensory-specific.

[1]  C. Gottesmann The neurophysiology of sleep and waking: intracerebral connections, functioning and ascending influences of the medulla oblongata , 1999, Progress in Neurobiology.

[2]  R. Blair,et al.  Convergence of multiple sensory inputs onto neurons in the dorsolateral medulla in cats , 1995, Neuroscience.

[3]  J. H. Fuller Brain stem reticular units: Some properties of the course and origin of the ascending trajectory , 1975, Brain Research.

[4]  J. Rauschecker,et al.  Centrifugal organization of direction preferences in the cat's lateral suprasylvian visual cortex and its relation to flow field processing , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  B. Jacobs,et al.  Raphe unit activity in freely moving cats: Effects of phasic auditory and visual stimuli , 1982, Brain Research.

[6]  M. Wallace,et al.  Superior colliculus neurons use distinct operational modes in the integration of multisensory stimuli. , 2005, Journal of neurophysiology.

[7]  A. Loewy,et al.  Brainstem projections to midline and intralaminar thalamic nuclei of the rat , 2002, The Journal of comparative neurology.

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

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

[11]  J. Siegel,et al.  Anatomical distribution and response patterns of reticular neurons active in relation to acoustic startle , 1988, Brain Research.

[12]  N. Logothetis,et al.  Integration of Touch and Sound in Auditory Cortex , 2005, Neuron.

[13]  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.

[14]  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.

[15]  Paul W. Frankland,et al.  The acoustic startle reflex: neurons and connections , 1995, Brain Research Reviews.

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

[17]  M. Meredith,et al.  On the neuronal basis for multisensory convergence: a brief overview. , 2002, Brain research. Cognitive brain research.

[18]  J. Siegel,et al.  Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movements. , 1983, Journal of neurophysiology.

[19]  Barry L. Jacobs,et al.  Single unit response of noradrenergic, serotonergic and dopaminergic neurons in freely moving cats to simple sensory stimuli , 1986, Brain Research.

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

[21]  M. Witter,et al.  The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness , 2002, Brain Research Reviews.

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

[23]  Christoph Kayser,et al.  Functional Imaging Reveals Visual Modulation of Specific Fields in Auditory Cortex , 2007, The Journal of Neuroscience.

[24]  D. Pfaff,et al.  Arousal of cerebral cortex electroencephalogram consequent to high-frequency stimulation of ventral medullary reticular formation , 2007, Proceedings of the National Academy of Sciences.

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

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

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

[28]  M Steriade,et al.  Neocortical and caudate projections of intralaminar thalamic neurons and their synaptic excitation from midbrain reticular core. , 1982, Journal of neurophysiology.

[29]  W. Singer,et al.  Role of Reticular Activation in the Modulation of Intracortical Synchronization , 1996, Science.

[30]  J. Siegel,et al.  Role of pontomedullary reticular formation neurons in horizontal head movements: an ibotenic acid lesion study in the cat , 1989, Brain Research.

[31]  John C Middlebrooks,et al.  Spatial sensitivity in the dorsal zone (area DZ) of cat auditory cortex. , 2005, Journal of neurophysiology.

[32]  D. Barth,et al.  Focal stimulation of the thalamic reticular nucleus induces focal gamma waves in cortex. , 1998, Journal of neurophysiology.

[33]  T. Imig,et al.  Binaural columns in the primary field (A1) of cat auditory cortex , 1977, Brain Research.

[34]  J. C. Middlebrooks,et al.  Binaural response-specific bands in primary auditory cortex (AI) of the cat: Topographical organization orthogonal to isofrequency contours , 1980, Brain Research.

[35]  Mark T. Wallace,et al.  Chapter 8 The visually responsive neuron and beyond: multisensory integration in cat and monkey , 1993 .

[36]  M. Koch,et al.  The neurobiology of startle , 1999, Progress in Neurobiology.

[37]  J. Lin,et al.  Brain structures and mechanisms involved in the control of cortical activation and wakefulness, with emphasis on the posterior hypothalamus and histaminergic neurons. , 2000, Sleep medicine reviews.

[38]  M. Merzenich,et al.  Responses of neurons in auditory cortex of the macaque monkey to monaural and binaural stimulation. , 1973, Journal of neurophysiology.

[39]  M Steriade,et al.  Arousal--Revisiting the Reticular Activating System , 1996, Science.

[40]  Liang Li,et al.  Tactile, acoustic and vestibular systems sum to elicit the startle reflex , 2002, Neuroscience & Biobehavioral Reviews.