Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields

Atiani, Serin; Elhilali, Mounya; David, Stephen V.; Fritz, Jonathan B.; Shamma, Shihab A.

doi:10.1016/j.neuron.2008.12.027

Cited by 204 publications

(240 citation statements)

References 30 publications

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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%

Mechanisms of noise robust representation of speech in primary auditory cortex

Mesgarani

David

Fritz

et al. 2014

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

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126

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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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Section: Discussionmentioning

confidence: 65%

Mechanisms of noise robust representation of speech in primary auditory cortex

Mesgarani

David

Fritz

et al. 2014

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

Self Cite

126

155

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“…This subcortical tuning likely results from a dynamic feedback system that includes both sensory and cognitive mechanisms interacting via bottom-up and top-down mechanisms (23). The OPERA hypothesis is corroborated by animal work showing that sound-to-meaning associations drive neural plasticity (3,42,43) and that feedback from cortical areas is necessary for learningrelated plasticity in subcortical regions (44). Thus, we propose that in humans, cognitive skills, including attention, may drive experience-dependent neural plasticity for behaviorally meaningful stimuli.…”

Section: Discussionmentioning

confidence: 87%

Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages

Krizman

Marian

Shook

et al. 2012

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

254

226

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Bilingualism profoundly affects the brain, yielding functional and structural changes in cortical regions dedicated to language processing and executive function [Crinion J, et al. (2006) Science 312:1537–1540; Kim KHS, et al. (1997) Nature 388:171–174]. Comparatively, musical training, another type of sensory enrichment, translates to expertise in cognitive processing and refined biological processing of sound in both cortical and subcortical structures. Therefore, we asked whether bilingualism can also promote experience-dependent plasticity in subcortical auditory processing. We found that adolescent bilinguals, listening to the speech syllable [da], encoded the stimulus more robustly than age-matched monolinguals. Specifically, bilinguals showed enhanced encoding of the fundamental frequency, a feature known to underlie pitch perception and grouping of auditory objects. This enhancement was associated with executive function advantages. Thus, through experience-related tuning of attention, the bilingual auditory system becomes highly efficient in automatically processing sound. This study provides biological evidence for system-wide neural plasticity in auditory experts that facilitates a tight coupling of sensory and cognitive functions.

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“…Recently, it has been successfully applied to neuroimaging data (Barnes et al, 2010;Rubinov and Sporns, 2011;Goulas et al, 2012).…”

Section: Methodsmentioning

confidence: 99%

“…Furthermore, as previous studies show that feature tuning in auditory cortex is highly affected by changes in task, context, and attention (Fritz et al, 2003;Atiani et al, 2009), the challenge for future work is to investigate changes in spectral profiles during these manipulations. Our results can guide future explorations of complex spectral tuning in human auditory cortex, and the methods described here provide a means for this endeavor.…”

Section: Neuronal Substrate Underlying Complex Population Tuningmentioning

confidence: 99%

Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex

Moerel

Martino

Santoro

et al. 2013

Journal of Neuroscience

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We examine the mechanisms by which the human auditory cortex processes the frequency content of natural sounds. Through mathematical modeling of ultra-high field (7 T) functional magnetic resonance imaging responses to natural sounds, we derive frequencytuning curves of cortical neuronal populations. With a data-driven analysis, we divide the auditory cortex into five spatially distributed clusters, each characterized by a spectral tuning profile. Beyond neuronal populations with simple single-peaked spectral tuning (grouped into two clusters), we observe that ϳ60% of auditory populations are sensitive to multiple frequency bands. Specifically, we observe sensitivity to multiple frequency bands (1) at exactly one octave distance from each other, (2) at multiple harmonically related frequency intervals, and (3) with no apparent relationship to each other. We propose that beyond the well known cortical tonotopic organization, multipeaked spectral tuning amplifies selected combinations of frequency bands. Such selective amplification might serve to detect behaviorally relevant and complex sound features, aid in segregating auditory scenes, and explain prominent perceptual phenomena such as octave invariance.

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Task Difficulty and Performance Induce Diverse Adaptive Patterns in Gain and Shape of Primary Auditory Cortical Receptive Fields

Cited by 204 publications

References 30 publications

Mechanisms of noise robust representation of speech in primary auditory cortex

Mechanisms of noise robust representation of speech in primary auditory cortex

Subcortical encoding of sound is enhanced in bilinguals and relates to executive function advantages

Processing of Natural Sounds: Characterization of Multipeak Spectral Tuning in Human Auditory Cortex

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