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Two Distinct Neural Timescales for Predictive Speech Processing.

ABSTRACT: During speech listening, the brain could use contextual predictions to optimize sensory sampling and processing. We asked if such predictive processing is organized dynamically into separate oscillatory timescales. We trained a neural network that uses context to predict speech at the phoneme level. Using this model, we estimated contextual uncertainty and surprise of natural speech as factors to explain neurophysiological activity in human listeners. We show, first, that speech-related activity is hierarchically organized into two timescales: fast responses (theta: 4-10 Hz), restricted to early auditory regions, and slow responses (delta: 0.5-4 Hz), dominating in downstream auditory regions. Neural activity in these bands is selectively modulated by predictions: the gain of early theta responses varies according to the contextual uncertainty of speech, while later delta responses are selective to surprising speech inputs. We conclude that theta sensory sampling is tuned to maximize expected information gain, while delta encodes only non-redundant information. VIDEO ABSTRACT.

SUBMITTER: Donhauser PW

PROVIDER: S-EPMC6981026 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Two Distinct Neural Timescales for Predictive Speech Processing.

Donhauser Peter W PW Baillet Sylvain S

Neuron 20191202 2

During speech listening, the brain could use contextual predictions to optimize sensory sampling and processing. We asked if such predictive processing is organized dynamically into separate oscillatory timescales. We trained a neural network that uses context to predict speech at the phoneme level. Using this model, we estimated contextual uncertainty and surprise of natural speech as factors to explain neurophysiological activity in human listeners. We show, first, that speech-related activity ...[more]

PMID: 31806493

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Project description:IntroductionWe examined which brain areas are involved in the comprehension of acoustically distorted speech using an experimental paradigm where the same distorted sentence can be perceived at different levels of intelligibility. This change in intelligibility occurs via a single intervening presentation of the intact version of the sentence, and the effect lasts at least on the order of minutes. Since the acoustic structure of the distorted stimulus is kept fixed and only intelligibility is varied, this allows one to study brain activity related to speech comprehension specifically.MethodsIn a functional magnetic resonance imaging (fMRI) experiment, a stimulus set contained a block of six distorted sentences. This was followed by the intact counterparts of the sentences, after which the sentences were presented in distorted form again. A total of 18 such sets were presented to 20 human subjects.ResultsThe blood oxygenation level dependent (BOLD)-responses elicited by the distorted sentences which came after the disambiguating, intact sentences were contrasted with the responses to the sentences presented before disambiguation. This revealed increased activity in the bilateral frontal pole, the dorsal anterior cingulate/paracingulate cortex, and the right frontal operculum. Decreased BOLD responses were observed in the posterior insula, Heschl's gyrus, and the posterior superior temporal sulcus.ConclusionsThe brain areas that showed BOLD-enhancement for increased sentence comprehension have been associated with executive functions and with the mapping of incoming sensory information to representations stored in episodic memory. Thus, the comprehension of acoustically distorted speech may be associated with the engagement of memory-related subsystems. Further, activity in the primary auditory cortex was modulated by prior experience, possibly in a predictive coding framework. Our results suggest that memory biases the perception of ambiguous sensory information toward interpretations that have the highest probability to be correct based on previous experience.

Project description:BackgroundFunctional near-infrared spectroscopy (fNIRS) studies have demonstrated associations between hearing outcomes after cochlear implantation and plastic brain changes. However, inconsistent results make it difficult to draw conclusions. A major problem is that many variables need to be controlled. To gain further understanding, a careful preparation and planning of such a functional neuroimaging task is key.ObjectiveUsing fNIRS, our main objective is to develop a well-controlled audiovisual speech comprehension task to study brain activation in individuals with normal hearing and hearing impairment (including cochlear implant users). The task should be deductible from clinically established tests, induce maximal cortical activation, use optimal coverage of relevant brain regions, and be reproducible by other research groups.MethodsThe protocol will consist of a 5-minute resting state and 2 stimulation periods that are 12 minutes each. During the stimulation periods, 13-second video recordings of the clinically established Oldenburg Sentence Test (OLSA) will be presented. Stimuli will be presented in 4 different modalities: (1) speech in quiet, (2) speech in noise, (3) visual only (ie, lipreading), and (4) audiovisual speech. Each stimulus type will be repeated 10 times in a counterbalanced block design. Interactive question windows will monitor speech comprehension during the task. After the measurement, we will perform a 3D scan to digitize optode positions and verify the covered anatomical locations.ResultsThis paper reports the study protocol. Enrollment for the study started in August 2021. We expect to publish our first results by the end of 2022.ConclusionsThe proposed audiovisual speech comprehension task will help elucidate neural correlates to speech understanding. The comprehensive study will have the potential to provide additional information beyond the conventional clinical standards about the underlying plastic brain changes of a hearing-impaired person. It will facilitate more precise indication criteria for cochlear implantation and better planning of rehabilitation.International registered report identifier (irrid)DERR1-10.2196/38407.

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Two Distinct Neural Timescales for Predictive Speech Processing.

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Two Distinct Neural Timescales for Predictive Speech Processing.

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