The pitch of vocalizations is a key communication feature aiding recognition of individuals and separating sound sources in complex acoustic environments. The neural representation of the pitch of periodic sounds is well defined. However, many natural sounds, like complex vocalizations, contain rich, aperiodic or not strictly periodic frequency content and/or include high‐frequency components, but still evoke a strong sense of pitch. Indeed, such sounds are the rule, not the exception but the cortical mechanisms for encoding pitch of such sounds are unknown. We investigated how neurons in the high‐frequency representation of primary auditory cortex (A1) of marmosets encoded changes in pitch of four natural vocalizations, two centred around a dominant frequency similar to the neuron's best sensitivity and two around a much lower dominant frequency. Pitch was varied over a fine range that can be used by marmosets to differentiate individuals. The responses of most high‐frequency A1 neurons were sensitive to pitch changes in all four vocalizations, with a smaller proportion of the neurons showing pitch‐insensitive responses. Classically defined excitatory drive, from the neuron's monaural frequency response area, predicted responses to changes in vocalization pitch in <30% of neurons suggesting most pitch tuning observed is not simple frequency‐level response. Moreover, 39% of A1 neurons showed call‐invariant tuning of pitch. These results suggest that distributed activity across A1 can represent the pitch of natural sounds over a fine, functionally relevant range, and exhibits pitch tuning for vocalizations within and outside the classical neural tuning area.
Based on anatomical connectivity and basic response characteristics, primate auditory cortex is divided into a central core surrounded by belt and parabelt regions. The encoding of pitch, a prototypical element of sound identity, has been studied in primary auditory cortex (A1) but little is known about how it is encoded and represented beyond A1. The caudal auditory belt and parabelt cortical fields process spatial information but also contain information on non-spatial aspects of sounds. In this study, we examined neuronal responses in these areas to pitch-varied marmoset vocalizations, to derive the consequent representation of pitch in these regions and the potential underlying mechanisms, to compare to the encoding and representation of pitch of the same sounds in A1. With respect to response patterns to the vocalizations, neurons in caudal medial belt (CM) showed similar short-latency and short-duration response patterns to A1, but caudal lateral belt (CL) neurons at the same hierarchical level and caudal parabelt (CPB) neurons at a higher hierarchical level showed delayed or much delayed response onset and prolonged response durations. With respect to encoding of pitch, neurons in all cortical fields showed sensitivity to variations in the vocalization pitch either through modulation of spike-count or of first spike-latency. The utility of the encoding mechanism differed between fields: pitch sensitivity was reliably represented by spike-count variations in A1 and CM, while first spike-latency variation was better for encoding pitch in CL and CPB. In summary, our data show that (a) the traditionally-defined belt area CM is functionally very similar to A1 with respect to the representation and encoding of complex naturalistic sounds, (b) the CL belt area, at the same hierarchical level as CM, and the CPB area, at a higher hierarchical level, have very different response patterns and appear to use different pitch-encoding mechanisms, and (c) caudal auditory fields, proposed to be specialized for encoding spatial location, can also contain robust representations of sound identity.
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