Research report
Multisensory auditory–somatosensory interactions in early cortical processing revealed by high-density electrical mapping

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Abstract

We investigated the time-course and scalp topography of multisensory interactions between simultaneous auditory and somatosensory stimulation in humans. Event-related potentials (ERPs) were recorded from 64 scalp electrodes while subjects were presented with auditory-alone stimulation (1000-Hz tones), somatosensory-alone stimulation (median nerve electrical pulses), and simultaneous auditory–somatosensory (AS) combined stimulation. Interaction effects were assessed by comparing the responses to combined stimulation with the algebraic sum of responses to the constituent auditory and somatosensory stimuli when they were presented alone. Spatiotemporal analysis of ERPs and scalp current density (SCD) topographies revealed AS interaction over the central/postcentral scalp which onset at approximately 50 ms post-stimulus presentation. Both the topography and timing of these interactions are consistent with multisensory integration early in the cortical processing hierarchy, in brain regions traditionally held to be unisensory.

Introduction

Unified perception of stimuli that are seen, felt and heard requires that regions of the brain receive convergent inputs from these different sensory modalities and that these convergent inputs are somehow integrated or ‘bound’. Such multisensory integration constitutes a fundamental component of cognition and behavior [26], [25]. The means by which information from the different sensory modalities is bound together in the brain is therefore of critical interest. Detailing the anatomic organization of the brain networks that subserve this integration will be crucial to our clarification of this aspect of the ‘binding’ problem. The temporal pattern of integration across the areas comprising these networks is key to understanding the nature of the interactions amongst these areas.

The objective of this study was to examine the time-course and scalp topography of multisensory integration processes between the senses of audition and somatosensation in humans. A number of recent studies have demonstrated the behavioral relevance of auditory–somatosensory (AS) interactions [8], [15], [24]. For instance, Jousmaki and Hari [8] have shown that artificially altering the rubbing sounds that subjects hear when they rub their hands together can drastically alter the tactile sensations that subjects report. In fact, by enhancing the high-frequency component (>2 kHz) of the rubbing sound, a majority of their subjects experienced the rather extraordinary sensation of having a leaf of parchment paper interposed between their rubbing hands. This effect underscores AS multisensory integration as an important adjunct to tactile judgements of texture. Also, recent evidence has shown that there are AS interactions during both focused and divided spatial attention tasks [15], [24].

Intracranial investigations in animals have identified candidate neural structures for such auditory–somatosensory (AS) integration. AS neurons have been found in the neostriatum and globus pallidus of the rat [1], superior colliculus [19], [32], [33] and anterior ectosylvian cortex of the cat [29], [28], [31], and the posterior parietal cortex [7], superior temporal sulcus [2], [6] and temporo-parietal cortex [11] of the monkey. In cats, multisensory AS neurons have also been described in the inferior colliculus, a subcortical relay to primary auditory cortices [27], although it is not clear to what extent these findings would apply to humans. Recent intracranial investigations in awake monkeys at this laboratory have shown AS co-representation in the posterior ‘belt’ region of macaque auditory cortex on the superior temporal plane [13]. Collectively, these findings suggest that AS integration may be a bottom-up (feed-forward) process occurring during initial sensory transmission and in early sensory cortices, which are usually assumed to be unisensory. Other potential areas for AS integration are lateral and ventral intraparietal sulcal areas (LIP [14], [21]and VIP [3]), both of which show audio–visual and somato–visual responses, but have not been directly investigated for AS function.

Since intracranial investigations in the superior temporal plane of awake macaques have shown early feedforward AS co-representation [13], we predicted integration effects during the timeframe of the earliest components of the human somatosensory and auditory-evoked responses (SEPs and AEPs). High-density event-related potential (ERP) recordings revealed multisensory AS interactions over the central/postcentral scalp region, contralateral to the side of multisensory stimulation that onset just 50 ms post-stimulus presentation.

Section snippets

Subjects

Eight (one female), neurologically normal, paid volunteers, aged 22–35 (mean=26.9±4.2) participated. All subjects provided written informed consent in accordance with the Declaration of Helsinki, and the procedures were approved by the Institutional Review Board of the Nathan Kline Institute for Psychiatric Research. All subjects reported having normal hearing, and were right-handed (except for one) as assessed by the Edinburgh handedness inventory.

Stimulation

Subjects were presented with three types of

Results

Inspection of the group-averaged voltage waveforms (see Fig. 1) over right central scalp (the expected scalp projection of both auditory and somatosensory cortices for left-sided stimulation) revealed a series of ERP components (N20, P30, P50, and N65) in the early time-period following auditory–somatosensory bi-sensory stimulus presentation (Figs. 1 and 2A).

A robust difference was noted between the responses to simultaneous AS stimulation and the summed responses from the separately presented

Discussion

This study revealed the presence of early interactions between the senses of somatosensation and audition in human subjects. Interaction effects were manifest by just 50 ms post-stimulus presentation. Scalp current density (SCD) topographic analysis revealed a central/post-central scalp distribution for the early phase of the interaction effect, contralateral to the side of stimulation. This distribution was largely consistent with interaction effects in somatosensory cortices in the region of

Conclusion

This study provides evidence for multisensory interactions between the senses of audition and somatosensation in human subjects. High-density 64-channel event-related potential recordings revealed significant differences between the responses to simultaneous bisensory auditory–somatosensory (AS) stimulation and the summed responses from auditory-alone and somatosensory-alone stimulation. These differences were seen by just 50 ms post-stimulus presentation over the scalp contralateral to the

Acknowledgements

Sincere appreciation to Robert Lindsley for technical support. Work supported by grants from the NIMH (MH1143 to JJF; MH49334 and MH01439 to DCJ).

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