Cortical voice processing is grounded in elementary sound analyses for vocalization relevant sound patterns

Staib, Matthias; Frühholz, Sascha

doi:10.1016/j.pneurobio.2020.101982

Cited by 11 publications

(22 citation statements)

References 53 publications

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“…This stands in contrast to functional neuroimaging work that used the NatS stimulus set to show that temporal voice regions may not exist (14). A recent study using artificially-generated sounds demonstrated that temporal voice regions may encode vocal perceptual quality, i.e., the extent to which a sound is voice-like (48). Since the environmental sounds stimuli do not sufficiently sample across this perceptual continuum, the current data are unable to shed light on this possibility directly.…”

Section: Discussioncontrasting

confidence: 84%

Categorical encoding of voice in human superior temporal cortex

Rupp

Hect

Remick

et al. 2021

Preprint

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The ability to recognize abstract features of voice during auditory perception is a complex, yet poorly understood, feat of human audition. For the listener, this occurs in near-automatic fasion to seamlessly extract complex cues from a highly variable auditory signal. Voice perception depends on specialized regions of auditory cortex, including superior temporal gyrus (STG) and superior temporal sulcus (STS). However, the nature of voice encoding at the cortical level remains poorly understoood. We leverage intracerebral recordings across human auditory cortex during presentation of voice and non-voice acoustic stimuli to examine voice encoding in auditory cortex, in eight patient-participants undergoing epilepsy surgery evaluation. We show that voice-selectivity increases along the auditory hierarchy from supratemporal plane (STP) to the STG and STS. Results show accurate decoding of vocalizations from human auditory cortical activity even in the complete absence of linguistic content. These findings show an early, less-selective temporal window of neural activity in the STG and STS followed by a sustained, strongly voice-selective window. We then developed encoding models that demonstrate divergence in the encoding of acoustic features along the auditory hierarchy, wherein STG/STS responses were best explained by voice category as opposed to the acoustic features of voice stimuli. This is in contrast to neural activity recorded from STP, in which responses were accounted for by acoustic features. These findings support a model of voice perception that engages categorical encoding mechanisms within STG and STS.Significance StatementVoice perception occurs via specialized networks in higher order auditory cortex, yet how voice features are encoded remains a central unanswered question. With human intracerebral recordings of auditory cortex, we provide evidence for categorical encoding of voice in STG and STS and occurs in the absence of linguistic content. This selectivity strengthens after an initial onset response and cannot be explained by simple acoustic features. Together, these data support the existence of sites within STG and STS that are specialized for voice perception.

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Section: Discussioncontrasting

confidence: 84%

Categorical encoding of voice in human superior temporal cortex

Rupp

Hect

Remick

et al. 2021

Preprint

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“…For the affective forced choice task, we created blends of vocally expressed anger and fear using a voice morphing procedure (Rauschecker and Scott 2009, Staib and Frühholz 2020) on a set of commonly available and validated vocal affective bursts, namely the Montreal affective voice database or ‘MAV’ (Belin, Fillion-Bilodeau et al 2008). From this database we selected five male and five female voices.…”

Section: Resultsmentioning

confidence: 99%

“…The neural processing and classification of acoustic information involves a cortical neural network beyond auditory decoding in the auditory cortex (AC; Staib and Frühholz 2020). The core of this neural network especially for decoding acoustic and social information conveyed by acoustic voice signals involves an integrated functioning of the AC together with various regions in the inferior frontal cortex (IFC; Rauschecker and Scott 2009, Roswandowitz, Swanborough et al 2020).…”

Section: Introductionmentioning

confidence: 99%

Disrupting inferior frontal cortex activity alters affect decoding efficiency from clear but not from ambiguous affective speech

Ceravolo

Moisa

Grandjean

et al. 2021

Preprint

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The evaluation of socio-affective sound information is accomplished by the primate neural auditory cortex in collaboration with limbic and inferior frontal brain nodes. For the latter, activity in inferior frontal cortex (IFC) is often observed during classification of voice sounds, especially if they carry affective information. Partly opposing views have been proposed, with IFC either coding cognitive processing challenges in case of sensory ambiguity or representing categorical object and affect information for clear vocalizations. Here, we presented clear and ambiguous affective speech to two groups of human participants during neuroimaging, while in one group we inhibited right IFC activity with transcranial magnetic stimulation (TMS) prior to brain scanning. Inhibition of IFC activity led to partly faster affective decisions, more accurate choice probabilities and reduced auditory cortical activity for clear affective speech, while fronto-limbic connectivity increased for clear vocalizations. This indicates that IFC inhibition might lead to a more intuitive and efficient processing of affect information in voices. Contrarily, normal IFC activity might represent a more deliberate form of affective sound processing (i.e., enforcing cognitive analysis) that flags categorial sound decisions with precaution (i.e., representation of categorial uncertainty). This would point to an intermediate functional property of the IFC between previously assumed mechanisms.TeaserInferior frontal cortex enforces cognitive analyses during affect decisions with different levels of sensory ambiguity.

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“…They suggested that the disparity between these results and previous fMRI work could be related to the relatively reduced granularity of fMRI approaches compared to sEEG. A recent fMRI study using artificially generated sounds demonstrated that temporal voice regions may encode vocal perceptual quality, i.e., the extent to which a sound is voice like [ 21 ]. Since the environmental sounds stimuli do not sufficiently sample across this perceptual continuum, the current data are unable to shed light on this possibility directly.…”

Section: Discussionmentioning

confidence: 99%

“…Whether activity in putative voice-selective areas of STG and STS is actually demonstrating selectivity for voice, and not the acoustic or linguistic properties of speech, remains under debate [ 12 , 20 , 21 ]. A speech-driven model of voice coding is supported by some neuroimaging studies [ 8 , 17 , 20 , 22 , 23 ].…”

Section: Introductionmentioning

confidence: 99%

Neural responses in human superior temporal cortex support coding of voice representations

et al. 2022

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The ability to recognize abstract features of voice during auditory perception is an intricate feat of human audition. For the listener, this occurs in near-automatic fashion to seamlessly extract complex cues from a highly variable auditory signal. Voice perception depends on specialized regions of auditory cortex, including superior temporal gyrus (STG) and superior temporal sulcus (STS). However, the nature of voice encoding at the cortical level remains poorly understood. We leverage intracerebral recordings across human auditory cortex during presentation of voice and nonvoice acoustic stimuli to examine voice encoding at the cortical level in 8 patient-participants undergoing epilepsy surgery evaluation. We show that voice selectivity increases along the auditory hierarchy from supratemporal plane (STP) to the STG and STS. Results show accurate decoding of vocalizations from human auditory cortical activity even in the complete absence of linguistic content. These findings show an early, less-selective temporal window of neural activity in the STG and STS followed by a sustained, strongly voice-selective window. Encoding models demonstrate divergence in the encoding of acoustic features along the auditory hierarchy, wherein STG/STS responses are best explained by voice category and acoustics, as opposed to acoustic features of voice stimuli alone. This is in contrast to neural activity recorded from STP, in which responses were accounted for by acoustic features. These findings support a model of voice perception that engages categorical encoding mechanisms within STG and STS to facilitate feature extraction.

show abstract

Cortical voice processing is grounded in elementary sound analyses for vocalization relevant sound patterns

Cited by 11 publications

References 53 publications

Categorical encoding of voice in human superior temporal cortex

Categorical encoding of voice in human superior temporal cortex

Disrupting inferior frontal cortex activity alters affect decoding efficiency from clear but not from ambiguous affective speech

Neural responses in human superior temporal cortex support coding of voice representations

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