Representation of a species-specific vocalization in the primary auditory cortex of the common marmoset: temporal and spectral characteristics

Abstract

1. The temporal and spectral characteristics of neural representations of a behaviorally important species-specific vocalization were studied in neuronal populations of the primary auditory cortex (A1) of barbiturate-anesthetized adult common marmosets (Callithrix jacchus), using both natural and synthetic vocalizations. The natural vocalizations used in electrophysiological experiments were recorded from the animals under study or from their conspecifics. These calls were frequently produced in vocal exchanges between members of our marmoset colony and are part of the well-defined and highly stereotyped vocal repertoire of this species. 2. The spectrotemporal discharge pattern of spatially distributed neuron populations in cortical field A1 was found to be correlated with the spectrotemporal acoustic pattern of a complex natural vocalization. However, the A1 discharge pattern was not a faithful replication of the acoustic parameters of a vocalization stimulus, but had been transformed into a more abstract representation than that in the auditory periphery. 3. Subpopulations of A1 neurons were found to respond selectively to natural vocalizations as compared with synthetic variations that had the same spectral but different temporal characteristics. A subpopulation responding selectively to a given monkey's call shared some but not all of its neuronal memberships with other individual-call-specific neuronal subpopulations. 4. In the time domain, responses of individual A1 units were phase-locked to the envelope of a portion of a complex vocalization, which was centered around a unit's characteristic frequency (CF). As a whole, discharges of A1 neuronal populations were phase-locked to discrete stimulus events but not to their rapidly changing spectral contents. The consequence was a reduction in temporal complexity and an increase in cross-population response synchronization. 5. In the frequency domain, major features of the stimulus spectrum were reflected in rate-CF profiles. The spectral features of a natural call were equally or more strongly represented by a subpopulation of A1 neurons that responded selectively to that call as compared with the entire responding A1 population. 6. Neuronal responses to a complex call were distributed very widely across cortical field A1. At the same time, the responses evoked by a vocalization scattered in discrete cortical patches were strongly synchronized to stimulus events and to each other. As a result, at any given time during the course of a vocalization, a coherent representation of the integrated spectrotemporal characteristics of a particular vocalization was present in a specific neuronal population. 7. These results suggest that the representation of behaviorally important and spectrotemporally complex species-specific vocalizations in A1 is 1) temporally integrated and 2) spectrally distributed in nature, and that the representation is carried by spatially dispersed and synchronized cortical cell assemblies that correspond to each individual's vocalizations in a specific and abstracted way.