Abstract

Using functional magnetic resonance imaging in awake behaving monkeys we investigated how species-specific vocalizations are represented in auditory and auditory-related regions of the macaque brain. We found clusters of active voxels along the ascending auditory pathway that responded to various types of complex sounds: inferior colliculus (IC), medial geniculate nucleus (MGN), auditory core, belt, and parabelt cortex, and other parts of the superior temporal gyrus (STG) and sulcus (STS). Regions sensitive to monkey calls were most prevalent in the anterior STG, but some clusters were also found in frontal and parietal cortex on the basis of comparisons between responses to calls and environmental sounds. Surprisingly, we found that spectrotemporal control sounds derived from the monkey calls (“scrambled calls”) also activated the parietal and frontal regions. Taken together, our results demonstrate that species-specific vocalizations in rhesus monkeys activate preferentially the auditory ventral stream, and in particular areas of the antero-lateral belt and parabelt.

Highlights

  • The concept of two streams in auditory cortical processing, analogous to that in visual cortex (Mishkin et al, 1983), was proposed more than a decade ago (Rauschecker, 1998a; Rauschecker and Tian, 2000)

  • We performed t-tests contrasting all sounds vs. baseline (“silence” trials), monkey vocalizations or calls (MC) vs. environmental sounds (Env), and MC vs. scrambled monkey calls (SMC)

  • While environmental sounds typically contain sharp temporal onsets, monkey vocalizations contain greater modulations in the spectral domain because of the harmonics contained in these sounds

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Summary

Introduction

The concept of two streams in auditory cortical processing, analogous to that in visual cortex (Mishkin et al, 1983), was proposed more than a decade ago (Rauschecker, 1998a; Rauschecker and Tian, 2000). The concept was supported by contrasting patterns of anatomical connections in the macaque from anterior/ventral and posterior/dorsal belt regions of auditory cortex to segregated domains of lateral prefrontal cortex (Romanski et al, 1999) and by different physiological properties of these belt regions. The anterior lateral belt (area AL) in the macaque exhibited enhanced selectivity for the identity of sounds (monkey vocalizations), whereas the caudal lateral belt (area CL) was selective to sound location (Tian et al, 2001; see Kusmierek and Rauschecker, 2014). An open question regarding the vocalization-processing network in the macaque brain is whether it carries information about the motor actions necessary to produce the vocalizations, as has been shown in humans listening to speech and music (Wilson et al, 2004; Leaver et al, 2009)

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