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• W2787776191 abstract "Institute of Neuroscience, Newcastle University MedicalSchool, Henry Wellcome Building, Newcastle uponTyne NE2 4HH, UKSummaryCommunicationsignalsareimportantforsocialinteractionsand survival and are thought to receivespecialized process-ing in the visual and auditory systems. Whereas the neuralprocessing of faces by face clusters and face cells hasbeen repeatedly studied [1–5], less is known about theneural representation of voice content. Recent functionalmagnetic resonance imaging (fMRI) studies have localizedvoice-preferring regions in the primate temporal lobe [6, 7],but the hemodynamic response cannot directly assessneurophysiological properties. We investigated the re-sponses of neurons in an fMRI-identified voice cluster inawake monkeys, and here we provide the first systematicevidence for voice cells. ‘‘Voice cells’’ were identified, inanalogy to ‘‘face cells,’’ as neurons responding at least2-fold stronger to conspecific voices than to ‘‘nonvoice’’sounds or heterospecific voices. Importantly, whereas faceclustersarethoughttocontainhighproportionsoffacecells[4] responding broadly to many faces [1, 2, 4, 5, 8–10], wefound that voice clusters contain moderate proportions ofvoice cells. Furthermore, individual voice cells exhibit highstimulus selectivity. The results reveal the neurophysiolog-ical bases for fMRI-defined voice clusters in the primatebrain and highlight potential differences in how the auditoryand visual systems generate selective representations ofcommunication signals.ResultsVocalizations are acoustically complex and richly informativecommunication signals. Many social animals are sensitive tovoice characteristics, implying that their brains can extractvoice content from the other acoustic features of communica-tionsounds(e.g.,vocalizationreferentialmeaning,calleraffec-tive state, etc.). For instance, in one setting, an animal mightdistinguish the voice of a conspecific from another class ofsounds (‘‘nonvoice’’), whereas in another setting, it might beimportanttodistinguish differentvoices.Asafirststeptowardadvancing our understanding of the neuronal processing ofvoice content, recent fMRI studies in humans and monkeyshave provided evidence for brain regions that stronglyrespond to voice-related content (e.g., see [6, 7]). However,thefMRIsignaldoesnotallowadirectassessmentofneuronalproperties [11]; thus, the neurophysiological underpinnings offMRI voice-preferring clusters remained unexplored. Further,it was not clear whether neuronal strategies for generatingselective representations of voices and faces might differ inthe auditory and visual systems, respectively [12].Visual studies of face-preferring cells have reported thatsingle neurons in the monkey inferior temporal lobe (1) exhibitstrongresponsestocategoriesoffaces(relativetoothercate-gories of objects), (2) appear to cluster in large proportions,and (3) are broadly responsive to different faces within thecategory of face stimuli (see [1, 2, 4, 5, 8–10]). We used fMRI-guided electrophysiology in two awake rhesus macaques(Macaca mulatta) to record from neurons in an fMRI voice-preferring cluster [7]. We observed evidence for single ‘‘voicecells’’ that (1) exhibit strong preferential responses to acategory of stimuli consisting of many conspecific voicesrelative to two other categories of acoustically matchednatural sounds, (2) appear to cluster in moderate proportions,and (3) have highly stimulus-selective responses. Theseresults highlight interesting potential divergences in howauditory or visual communication signals are representedin the primate brain.To study neuronal voice-related processing, we used threecarefully controlled categories of complex natural sounds forstimulation: (1) macaque calls from 12 different callers(MVocs),(2)otheranimalcallsfrom12differentcallers(AVocs),and (3) 12 natural environmental sounds (NSnds). Motivatedfrom the study of face-preferring cells that have evaluatedneuronalresponsesto‘‘face’’versus‘‘nonface’’stimuluscate-gories [1–5, 8–10], a key goal of our study was the comparisonof neuronal responses to the voice (MVocs) versus thenonvoice (NSnds) stimulus categories, including how theseauditory results might compare to those for visual face cells.The AVocs category was included to provide additional infor-mation about whether the distinction of conspecific voices(MVocs)versus heterospecific voices (AVocs) might be impor-tant, as previous fMRI results on voice preference havesuggested[7,13].These36stimuliweresampledfromalargerset of sounds using the following criteria: we required thateach of the vocalizations in the MVocs and AVocs categorieswere produced by different callers (i.e., many voices) andthat the sound categories did not significantly differ in at leasttwo key acoustical features (i.e., the overall frequency spec-trum and modulations in the temporal envelope; for detailssee Figures S1A and S1B available online; SupplementalExperimentalProcedures).Inpractice,matchingtheacousticsacross the stimulus categories necessitated that the samplingof MVocs and AVocs stimulus sets included acousticallydistinct types of commonly produced calls (as opposed tosampling only one or a few call types). Nonetheless, becausewe constrained our MVocs to consist of multiple call-typeexemplars produced by different individuals, we could sepa-rately analyze the impact of ‘‘call-type’’ and ‘‘voice’’ factorson the neuronal responses (see below).The targeted voice-preferring fMRI cluster resides inhierarchically high-level auditory cortex on the supratemporal" @default.
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• W2787776191 date "2011-01-01" @default.
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• W2787776191 title "Report Voice Cells in the Primate Temporal Lobe" @default.
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