Abstract
Vocalizations are behaviorally critical sounds, and this behavioral importance is reflected in the ascending auditory system, where conspecific vocalizations are increasingly over-represented at higher processing stages. Recent evidence suggests that, in macaques, this increasing selectivity for vocalizations might culminate in a cortical region that is densely populated by vocalization-preferring neurons. Such a region might be a critical node in the representation of vocal communication sounds, underlying the recognition of vocalization type, caller and social context. These results raise the questions of whether cortical specializations for vocalization processing exist in other species, their cortical location, and their relationship to the auditory processing hierarchy. To explore cortical specializations for vocalizations in another species, we performed high-field fMRI of the auditory cortex of a vocal New World primate, the common marmoset (Callithrix jacchus). Using a sparse imaging paradigm, we discovered a caudal-rostral gradient for the processing of conspecific vocalizations in marmoset auditory cortex, with regions of the anterior temporal lobe close to the temporal pole exhibiting the highest preference for vocalizations. These results demonstrate similar cortical specializations for vocalization processing in macaques and marmosets, suggesting that cortical specializations for vocal processing might have evolved before the lineages of these species diverged.
Highlights
Vocalizations are behaviorally critical sounds, and this behavioral importance is reflected in the ascending auditory system, where conspecific vocalizations are increasingly over-represented at higher processing stages
This increasing representational bias for conspecific vocalizations appears to culminate in a cortical region located in the anterior auditory cortex that is densely populated with neurons that preferentially respond to conspecific vocalizations[9,10,11,12]
We asked whether the auditory cortex of the common marmoset (Callithrix jacchus), a New World primate that last shared a common ancestor with the macaque lineage about 40 million years ago[13,14], exhibits similar functional hierarchies for vocalization processing, and where they are localized in the brain
Summary
Vocalizations are behaviorally critical sounds, and this behavioral importance is reflected in the ascending auditory system, where conspecific vocalizations are increasingly over-represented at higher processing stages. Higher in the processing hierarchy, greater selectivity for individual vocalizations is achieved by single neurons in rostral/anterior cortex[7,8] In macaque monkeys, this increasing representational bias for conspecific vocalizations appears to culminate in a cortical region located in the anterior auditory cortex that is densely populated with neurons that preferentially respond to conspecific vocalizations[9,10,11,12]. This increasing representational bias for conspecific vocalizations appears to culminate in a cortical region located in the anterior auditory cortex that is densely populated with neurons that preferentially respond to conspecific vocalizations[9,10,11,12] The existence of such a vocalization-selective region in macaques raises the question of whether other species exhibit similar hierarchies or cortical specializations for vocalization processing, and whether similar brain structures are involved in these specializations. Our results demonstrate that similar structure-function relationships might operate in marmosets and macaques for vocalization coding, and provide a basis for detailed studies of marmoset temporal pole regions using electrophysiological and high-resolution imaging methods to probe the neural basis of the processing of vocal communication sounds
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