The multisensory roles for auditory cortex in primate vocal communication

Abstract

Primate vocal communication is a fundamentally multisensory behavior and this will be reflected in the different roles brain regions play in mediating it. Auditory cortex is illustrative, being influenced, I will argue, by the visual, somatosensory, proprioceptive and motor modalities during vocal communication. It is my intention that the data reviewed here suggest that investigating auditory cortex through the lens of a specific behavior may lead to a much clearer picture of its functions and dynamic organization. One possibility is that, beyond its tonotopic and cytoarchitectural organization, the auditory cortex may be organized according to ethologically-relevant actions. Such action-specific representations would be overlayed on top of traditional mapping schemes and would help mediate motor and multisensory processes related to a particular type of behavior.

Figure 1

Exemplars of the facial expressions produced concomitantly with vocalizations. A. Rhesus monkey coo and scream calls taken at the midpoint of the expressions with their corresponding spectrograms.

Figure 2

Single neuron examples of multisensory integration of Face+Voice stimuli compared with Disk+Voice stimuli in the middle lateral (ML) belt area. The left panel shows an enhanced response when voices are coupled with faces, but no similar modulation when coupled with disks. The right panel shows similar effects for a suppressed response. x-axes show time aligned to onset of the face (solid line). Dashed lines indicate the onset and offset of the voice signal. y-axes depict the firing rate of the neuron in spikes per second. Shaded regions denote the SEM.

Figure 3

A. Time-frequency plots (cross-spectrograms) illustrate the modulation of functional interactions (as a function of stimulus condition) between the lateral belt auditory cortex and the STS for a population of cortical sites. X-axes depict the time in milliseconds as a function of onset of the auditory signal (solid black line). Y-axes depict the frequency of the oscillations in Hz. Color-bar indicates the amplitude of these signals normalized by the baseline mean. B. Population phase concentration from 0-300ms after voice onset. X-axes depict frequency in Hz. Y axes depict the average normalized phase concentration. Shaded regions denote the SEM across all electrode pairs and calls. All values are normalized by the baseline mean for different frequency bands. Right panel shows the phase concentration across all calls and electrode pairs in the gamma band for the four conditions. C. Spike-field cross-spectrogram illustrates the relationship between the spiking activity of auditory cortical neurons and the STS local field potential across the population of cortical sites. X axes depict time in milliseconds as a function of the onset of the multisensory response in the auditory neuron (solid black line). Y-axes depict the frequency in Hz. Color-bar denotes the cross-spectral power normalized by the baseline mean for different frequencies.

Figure 4

A. The average fixation on the eye region versus the mouth region across three subjects while viewing a 30-sec video of vocalizing conspecific. The audio track had no influence on the proportion of fixations falling onto the mouth or the eye region. Error bars represent SEM. B. We also find that when monkeys do saccade to the mouth region, it is tightly correlated with the onset of mouth movements (r = 0.997, p <0.00001).

Figure 5

A. Examples of cutaneous receptive fields of neurons recorded in auditory cortical area CM B. Proportions of different types of somatosensory receptive fields recorded from auditory cortical area CM. x-axis is percentage of multiunit sites. (Both figures redrawn from Fu et al, 2003)