Interareal and interlaminar differences in sound envelope encoding in core and parabelt auditory cortex
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Amplitude-modulation (AM) plays an important role in the perception of complex sounds, and transformations in AM encoding may underlie aspects of complex sound perception. Previous studies have described a hierarchical progression across the auditory pathway, characterized by a decrease in the temporal precision of AM encoding. In human and nonhuman primates (NHP), the left hemisphere exhibits enhanced temporal encoding relative to the right hemisphere. The NHP model provides an opportunity to understand what circuit mechanisms generate these transformations in encoding by characterizing AM encoding in different intracortical circuits, and across the cortical hierarchy. To address this, here we report the encoding of AM signals as a function of cortical layer and hemisphere in NHP core and parabelt auditory cortex (AC). We recorded electrophysiological activity using linear array multielectrodes positioned across cortical layers while AM noise and click trains were presented to awake NHPs. Core AC typically encoded all AM frequencies (1.6-200 Hz) with high (> 90%) classification accuracy, while sites in the parabelt encoded a subset of lower (∼1.6-25 Hz) frequencies. Across both areas, the granular and infragranular layers displayed enhanced AM encoding relative to the supragranular layers. Both areas displayed enhanced AM encoding in the left hemisphere, restricted to the supragranular layers. These results represent the first analysis of AM encoding in the parabelt, indicating that significant temporal encoding of AM is still present in tertiary auditory cortex, and the layer-specific hemispheric differences suggest a potential supragranular layer origin of previously documented left-hemisphere dominance in temporal encoding.
Significance Statement
The loudness of natural sounds fluctuate rapidly – a feature known as amplitude modulation (AM). The rate of AM allows us to differentiate the pitch of different voices, discriminate speech from music, and supports other foundational aspects of perception. This study investigated AM encoding in specific intracortical circuits across levels of auditory cortex. We demonstrate here that each level of the hierarchy displays enhanced encoding in the deep cortical layers relative to the superficial layers. We also observed that the left hemisphere dominance in AM encoding, evident in humans and nonhuman primates, was localized mainly to the superficial layers. This provides new understanding of how the third level of the nonhuman primate cortical hierarchy, the parabelt, encodes complex stimuli.
