Somatosensory Input to Auditory Association Cortex in the Macaque Monkey

Abstract

We investigated the convergence of somatosensory and auditory inputs in within subregions of macaque auditory cortex. Laminar current source density and multiunit activity profiles were sampled with linear array multielectrodes during penetrations of the posterior superior temporal plane in three macaque monkeys. At each recording site, auditory responses to binaural clicks, pure tones, and band-passed noise, all presented by earphones, were compared with somatosensory responses evoked by contralateral median nerve stimulation. Subjects were awake but were not required to discriminate the stimuli. Borders between A1 and surrounding belt regions were identified by mapping best frequency and stimulus preferences and by subsequent histological analysis. Regions immediately caudomedial to A1 had robust somatosensory responses co-represented with auditory responses. In these regions, both somatosensory and auditory response profiles had "feedforward" patterns; initial excitation beginning in Lamina 4 and spreading to extragranular laminae. Auditory and somatosensory responses displayed a high degree of temporal overlap. Anatomical reconstruction indicated that the somatosensory input region includes, but may not be restricted to, the caudomedial auditory association cortex. As was earlier reported for this region, auditory frequency tuning curves were broad and band-passed noise responses were larger than pure tone responses. No somatosensory responses were observed in A1. These findings suggest a potential neural substrate for multisensory integration at an early stage of auditory cortical processing.

Multisensory anatomical pathways

“…These recent results were highly complementary to the pioneer works of Schroeder's laboratory that have revealed the multimodal feature of the monkey auditory belt where both visual and somatosensory responses can be evoked (Schroeder et al, 2001;Schroeder and Foxe, 2002;Fu et al, 2003). In the carnivore, while previous studies have reported that the visual cortex can be activated by auditory stimuli (Spinelli et al, 1968;Morrell, 1972;Fishman and Michael, 1973), intracellular recording in the primary visual cortex (A17) have recently failed to find such auditory responses (Sanchez-Vives et al, 2006).…”

“…Although somewhat surprising, there is evidence for the existence of multisensory neurons in areas traditionally considered as unisensory, such as the visual cortex (between areas 17 and 18a) in the rat (Barth et al, 1995) and in the auditory cortex of the monkey (Watanabe and Iwai, 1991;Schroeder et al, 2001;Cappe et al, 2007b;Kayser et al, 2008) and of the ferret (Bizley et al, 2007;Bizley and King, 2008). In addition, previous studies have shown the existence of scattered projections of the auditory cortex towards the visual area 18 in the rat and the cat (Miller and Vogt, 1984;Innocenti et al, 1988).…”

“…The notion that multisensory integration is restricted to higherorder areas has recently been challenged by human and animal studies that have revealed that crossmodal interactions can occur in unisensory areas at very low levels of cortical processing (Buchel et al, 1998;Calvert et al, 1999Calvert et al, , 2001Macaluso et al, 2000;Schroeder et al, 2001;Amedi et al, 2002;Ghazanfar et al, 2005;Kriegstein et al, 2005;Miller and D'Esposito, 2005;Watkins et al, 2006;Martuzzi et al, 2007;Kayser et al, 2007Kayser et al, , 2008Romei et al, 2007Romei et al, , 2008Wang et al, 2008) and more importantly at very short latencies (Giard and Peronnet, 1999;Foxe et al, 2000;Molholm et al, 2002;Murray et al, 2005;Senkowski et al, 2007;Sperdin et al, 2009). Such a fast timing of multisensory interactions rule out an origin in the multisensory areas mediated through backward projections, and instead favor direct heteromodal connections.…”

Structural changes of the corpus callosum in tinnitus

“…The hypothetical mechanism underlying a putative protective function may relate to the fact that the playing of an instrument generates regularly patterned and correlated reafferent input streams to the auditory and the somatosensory system. There are multiple somatosensory entries into the auditory system that are capable of modulating auditory cortex activity (Schroeder et al, 2001; Lakatos et al, 2007). Increase of auditory cortex size and enhancement of fiber projections through the anterior CC may represent components of a protective auditory-motor-somatosensory-auditory loop.…”

Gamma and beta neural activity evoked during a sensory gating paradigm: Effects of auditory, somatosensory and cross-modal stimulation

“…Given the extant literature on multisensory integration, a cross-modal sensory gating effect was not unexpected here. For example, the presence of both anatomical substrates (Schroeder et al, 2001) and functional interactions (Brett-Green et al, 2004;Foxe et al, 2002) between auditory and somatosensory modalities has been demonstrated at the cortical level. The latter includes scalp-recorded neurophysiological effects on the same time-scale (<100 ms) as that observed here (Foxe et al, 2000;Murray et al, 2005).…”