Cortical activity patterns predict speech discrimination ability

Perez, Claudia; Chen, Ye Ting H.; Carraway, Ryan S.; Reed, Amanda C.; Shetake, Jai A.; Jakkamsetti, Vikram; Chang, Kevin Q.; Kilgard, Michael P.

doi:10.1038/nn.2109

Cited by 187 publications

(405 citation statements)

References 50 publications

(47 reference statements)

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“…The decoding performance was best when short time bins were used to sample the response, revealing that the temporal structure of the neurons responses (not just the response magnitude) provides information to distinguish individual sounds. In this respect, insula neurons resemble those found in auditory cortex (Schnupp et al, 2006;Engineer et al, 2008).…”

Section: Selectivity To Individual Vocalizationssupporting

confidence: 52%

An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds

Remedios¹,

Logothetis²,

Kayser³

2009

J. Neurosci.

126

100

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Human imaging studies implicate the insular cortex in processing complex sounds and vocal communication signals such as speech. In addition, lesions of the insula often manifest as deficits in sound or speech recognition (auditory agnosia) and speech production. While models of acoustic perception assign an important role to the insula, little is known about the underlying neuronal substrate. Studying a vocal primate, we identified a predominantly auditory region in the caudal insula and therein discovered a neural representation of conspecific communication sounds. When probed with natural sounds, insula neurons exhibited higher response selectivity than neurons in auditory cortex, and in contrast to these, responded preferentially to conspecific vocalizations. Importantly, insula neurons not only preferred conspecific vocalizations over a wide range of environmental sounds and other animal vocalizations, but also over acoustically manipulated versions of these, demonstrating that this preference for vocalizations arises both from spectral and temporal features of the sounds. In addition, individual insula neurons responded highly selectively to only a few vocalizations and allowed the decoding of sound identity from single-trial responses. These findings characterize the caudal insula as a selectively responding auditory region, possibly part of a processing stream involved in the representation of communication sounds. Importantly, our results provide a neural counterpart for the human imaging and lesion findings and uncover a basis for a supposed role of the insula in processing vocal communication sounds such as speech.

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Section: Selectivity To Individual Vocalizationssupporting

confidence: 52%

An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds

Remedios¹,

Logothetis²,

Kayser³

2009

J. Neurosci.

126

100

View full text Add to dashboard Cite

show abstract

“…For example, trained rats were shown to being able to report millisecond differences in patterns of electrical microstimulation applied to auditory cortex (31), demonstrating that auditory cortex can access temporally precise patterns of local activity. In addition, another study demonstrated that behavioral performance can be better explained when decoding neural population activity sampled at a precision well below 10 ms than when decoding the same responses at coarser time scales (32). The present results demonstrate that the responses of individual neurons can indeed contribute to such millisecond encoding of complex sounds.…”

Section: Discussionmentioning

confidence: 50%

Millisecond encoding precision of auditory cortex neurons

Kayser

Logothetis

Panzeri

2010

Proc. Natl. Acad. Sci. U.S.A.

118

120

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Neurons in auditory cortex are central to our perception of sounds. However, the underlying neural codes, and the relevance of millisecond-precise spike timing in particular, remain debated. Here, we addressed this issue in the auditory cortex of alert nonhuman primates by quantifying the amount of information carried by precise spike timing about complex sounds presented for extended periods of time (random tone sequences and natural sounds). We investigated the dependence of stimulus information on the temporal precision at which spike times were registered and found that registering spikes at a precision coarser than a few milliseconds significantly reduced the encoded information. This dependence demonstrates that auditory cortex neurons can carry stimulus information at high temporal precision. In addition, we found that the main determinant of finely timed information was rapid modulation of the firing rate, whereas higher-order correlations between spike times contributed negligibly. Although the neural coding precision was high for random tone sequences and natural sounds, the information lost at a precision coarser than a few milliseconds was higher for the stimulus sequence that varied on a faster time scale (random tones), suggesting that the precision of cortical firing depends on the stimulus dynamics. Together, these results provide a neural substrate for recently reported behavioral relevance of precisely timed activity patterns with auditory cortex. In addition, they highlight the importance of millisecond-precise neural coding as general functional principle of auditory processing-from the periphery to cortex.hearing | neural code | spike timing | natural sounds | mutual information O ur auditory system can reliably encode natural sounds that vary simultaneously over many time scales, and from these sounds, it can extract behaviorally relevant information such as a speaker's identity or the sound qualities of musical instruments (1, 2). Neurons in the auditory cortex are sensitive to temporally structured acoustic stimuli and likely play a central role in mediating their perception (3). Yet, how exactly auditory cortex neurons use their temporal patterns of action potentials (spikes) to provide an information-rich representation of complex or natural sounds remains debated.One central question pertains to the relevance of millisecondprecise spike times of individual auditory cortical neurons for stimulus encoding. Previous work has shown that onset responses to isolated brief sounds can be millisecond-precise and carry acoustic information (4-6). However, auditory cortex neurons cannot lock their responses to rapid sequences of short stimuli. For example, during the repetitive presentation of brief sounds, their response precision degrades when the intersound interval becomes shorter than ≈10-20 ms. This finding argues against a role of millisecond-precise spike timing in the encoding of fast sequences of short sounds (7,8). In addition, studies on the decoding of complex sounds from single-tria...

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“…Although we cannot conclude that the neurophysiological response properties we have described here are necessarily essential for behavior, several existing studies using synthetic stimuli (34) and speech (23) have demonstrated that ferrets and rodents are able to perceive target sounds in noisy conditions similar to those used in this study. The functional properties observed for speech and conspecific vocalizations in distorted conditions may reflect computational strategies used in these behaviors, and future studies that combine our unique computational approach and behavior paradigms promise valuable new insight into the general problem of identifying signals in the background of interfering sources (5).…”

Section: Discussionmentioning

confidence: 65%

“…Their robust representations in neural data are therefore crucial for speech comprehension. As with other natural sounds, it is likely that basic neural mechanisms contribute to the stability and robustness of their representations in early stages of auditory processing (23). To examine the effect of distortions on phoneme category representation, we measured the mean phoneme spectrograms averaged over all of the instances of individual phonemes (24).…”

Section: Reduced Distortions In Stimuli Reconstructed From the A1 Popmentioning

confidence: 99%

Mechanisms of noise robust representation of speech in primary auditory cortex

Mesgarani

David

Fritz

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

121

155

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Humans and animals can reliably perceive behaviorally relevant sounds in noisy and reverberant environments, yet the neural mechanisms behind this phenomenon are largely unknown. To understand how neural circuits represent degraded auditory stimuli with additive and reverberant distortions, we compared single-neuron responses in ferret primary auditory cortex to speech and vocalizations in four conditions: clean, additive white and pink (1/f) noise, and reverberation. Despite substantial distortion, responses of neurons to the vocalization signal remained stable, maintaining the same statistical distribution in all conditions. Stimulus spectrograms reconstructed from population responses to the distorted stimuli resembled more the original clean than the distorted signals. To explore mechanisms contributing to this robustness, we simulated neural responses using several spectrotemporal receptive field models that incorporated either a static nonlinearity or subtractive synaptic depression and multiplicative gain normalization. The static model failed to suppress the distortions. A dynamic model incorporating feedforward synaptic depression could account for the reduction of additive noise, but only the combined model with feedback gain normalization was able to predict the effects across both additive and reverberant conditions. Thus, both mechanisms can contribute to the abilities of humans and animals to extract relevant sounds in diverse noisy environments.hearing | cortical | population code | phonemes V ocal communication in the real world often takes place in complex, noisy acoustic environments. Although substantial effort is required to perceive speech in extremely noisy conditions, accurate perception in moderately noisy and reverberant environments is relatively effortless (1), presumably because of the presence of general filtering mechanisms in the auditory pathway (2). These mechanisms likely influence the representation and perception of both speech and other natural sounds with similarly rich spectrotemporal structure, such as species-specific vocalizations (3-5). Despite the central role this robustness must play in animal and human hearing, little is known about the underlying neural mechanisms and whether the brain maintains invariant representations of these stimuli across variable soundscapes causing acoustic distortions of the original signals.Several theoretical and experimental studies have postulated that the distribution of linear spectrotemporal tuning of neurons found in the auditory pathway could support enhanced representation of temporal and spectral modulations matched to those prevalent in natural stimuli (6, 7). Others have attributed this effect to nonlinear response properties of neurons (8) and adaptation with various timescales (9). In this study, we tested the noise robustness of auditory cortical neurons by recording responses in ferret primary auditory cortex (A1) to natural vocalizations that were distorted by additive white and pink (1/f) noise or by convolutive reverber...

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Cortical activity patterns predict speech discrimination ability

Cited by 187 publications

References 50 publications

An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds

An Auditory Region in the Primate Insular Cortex Responding Preferentially to Vocal Communication Sounds

Millisecond encoding precision of auditory cortex neurons

Mechanisms of noise robust representation of speech in primary auditory cortex

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