Cross-modal circuitry between auditory and somatosensory areas of the cat anterior ectosylvian sulcal cortex: a 'new' inhibitory form of multisensory convergence.

Abstract

Examples of convergence of visual and auditory, or visual and somatosensory, inputs onto individual neurons abound throughout the brain, but substantially fewer incidences of auditory-somatosensory neurons have been reported. The present experiments sought to examine auditory-somatosensory convergence to assess whether there is a feature of this type of convergence that might obscure it from conventional methods of multisensory detection. Auditory-somatosensory convergence was explored in cat anterior ectosylvian sulcus (AES) cortex, where higher-order somatosensory area IV (SIV) and auditory field of the anterior ectosylvian sulcus (FAES) share a common border. While neuroanatomical tracers documented a projection from FAES to SIV, physiological studies failed to reveal the bimodal neurons expected from such cross-modal connectivity. Stimulation of FAES through indwelling electrodes also failed to excite any of the SIV neurons examined. However, when stimulation of auditory FAES was combined with somatosensory stimulation, a large majority (66%) of SIV neurons showed a significant response attenuation. FAES-induced response suppression was specific to SIV, could not be elicited by activating other auditory regions and was blocked by the microiontophoretic application of the GABAergic antagonist bicuculline methiodide. Based on these data, a novel, cross-modal circuit is proposed involving projections from auditory FAES to somatosensory SIV, where local inhibitory interneurons 'reverse the sign' of the cross-modal signals to produce auditory-somatosensory suppression. This form of excitatory-inhibitory multisensory convergence has not been reported before and suggests that the level of interaction between auditory and somatosensory modalities has been substantially underestimated.