Common or redundant neural circuits for duration processing across audition and touch

Abstract

Certain features of objects or events can be represented by more than a single sensory system, such as roughness of a surface (sight, sound, and touch), the location of a speaker (audition and sight), and the rhythm or duration of an event (by all three major sensory systems). Thus, these properties can be said to be sensory-independent or amodal. A key question is whether common multisensory cortical regions process these amodal features, or does each sensory system contain its own specialized region(s) for processing common features? We tackled this issue by investigating simple duration-detection mechanisms across audition and touch; these systems were chosen because fine duration discriminations are possible in both. The mismatch negativity (MMN) component of the human event-related potential provides a sensitive metric of duration processing and has been elicited independently during both auditory and somatosensory investigations. Employing high-density electroencephalographic recordings in conjunction with intracranial subdural recordings, we asked whether fine duration discriminations, represented by the MMN, were generated in the same cortical regions regardless of the sensory modality being probed. Scalp recordings pointed to statistically distinct MMN topographies across senses, implying differential underlying cortical generator configurations. Intracranial recordings confirmed these noninvasive findings, showing generators of the auditory MMN along the superior temporal gyrus with no evidence of a somatosensory MMN in this region, whereas a robust somatosensory MMN was recorded from postcentral gyrus in the absence of an auditory MMN. The current data clearly argue against a common circuitry account for amodal duration processing.

Figure 1.

Grand mean ERPs for the somatosensory (Soma) and auditory (Audio) conditions at the frontocentral site, Fz, for deviant (50 ms; red line), standard (100 ms; green line), and the subtraction waveform (mismatch, black line). The times indicate the midpoint latencies of the 40 ms windows over which the average amplitude of the MMNs were measured.

Figure 2.

Topographical plots of the grand average mismatch waves for each modality (row) and each phase (column). The MMN is plotted at peak latency for each modality at the two different phases. The TANOVA tested for topographical differences at each time point between the sMMN and the aMMN.

Figure 3.

Grand mean CSD, at intracranial electrodes sites deviant (red line), standard (green line), and the subtraction waveform, MMN (black and gray lines). The yellow and magenta dots represent the electrode locations on the MRI-CTs. The yellow and magenta arrows indicate the Sylvian fissure and the postcentral gyrus, respectively.