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Primary auditory cortex representation of fear‐conditioned musical sounds


Staib, Matthias; Abivardi, Aslan; Bach, Dominik R (2020). Primary auditory cortex representation of fear‐conditioned musical sounds. Human Brain Mapping, 41(4):882-891.

Abstract

Auditory cortex is required for discriminative fear conditioning beyond the classical amygdala microcircuit, but its precise role is unknown. It has previously been suggested that Heschl's gyrus, which includes primary auditory cortex (A1), but also other auditory areas, encodes threat predictions during presentation of conditioned stimuli (CS) consisting of monophones, or frequency sweeps. The latter resemble natural prosody and contain discriminative spectro-temporal information. Here, we use functional magnetic resonance imaging (fMRI) in humans to address CS encoding in A1 for stimuli that contain only spectral but no temporal discriminative information. Two musical chords (complex) or two monophone tones (simple) were presented in a signaled reinforcement context (reinforced CS+ and nonreinforced CS-), or in a different context without reinforcement (neutral sounds, NS1 and NS2), with an incidental sound detection task. CS/US association encoding was quantified by the increased discriminability of BOLD patterns evoked by CS+/CS-, compared to NS pairs with similar physical stimulus differences and task demands. A1 was defined on a single-participant level and based on individual anatomy. We find that in A1, discriminability of CS+/CS- was higher than for NS1/NS2. This representation of unconditioned stimulus (US) prediction was of comparable magnitude for both types of sounds. We did not observe such encoding outside A1. Different from frequency sweeps investigated previously, musical chords did not share representations of US prediction with monophone sounds. To summarize, our findings suggest decodable representation of US predictions in A1, for various types of CS, including musical chords that contain no temporal discriminative information.

Abstract

Auditory cortex is required for discriminative fear conditioning beyond the classical amygdala microcircuit, but its precise role is unknown. It has previously been suggested that Heschl's gyrus, which includes primary auditory cortex (A1), but also other auditory areas, encodes threat predictions during presentation of conditioned stimuli (CS) consisting of monophones, or frequency sweeps. The latter resemble natural prosody and contain discriminative spectro-temporal information. Here, we use functional magnetic resonance imaging (fMRI) in humans to address CS encoding in A1 for stimuli that contain only spectral but no temporal discriminative information. Two musical chords (complex) or two monophone tones (simple) were presented in a signaled reinforcement context (reinforced CS+ and nonreinforced CS-), or in a different context without reinforcement (neutral sounds, NS1 and NS2), with an incidental sound detection task. CS/US association encoding was quantified by the increased discriminability of BOLD patterns evoked by CS+/CS-, compared to NS pairs with similar physical stimulus differences and task demands. A1 was defined on a single-participant level and based on individual anatomy. We find that in A1, discriminability of CS+/CS- was higher than for NS1/NS2. This representation of unconditioned stimulus (US) prediction was of comparable magnitude for both types of sounds. We did not observe such encoding outside A1. Different from frequency sweeps investigated previously, musical chords did not share representations of US prediction with monophone sounds. To summarize, our findings suggest decodable representation of US predictions in A1, for various types of CS, including musical chords that contain no temporal discriminative information.

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Additional indexing

Item Type:Journal Article, refereed, original work
Communities & Collections:04 Faculty of Medicine > Psychiatric University Hospital Zurich > Clinic for Psychiatry, Psychotherapy, and Psychosomatics
Dewey Decimal Classification:610 Medicine & health
Scopus Subject Areas:Health Sciences > Anatomy
Health Sciences > Radiological and Ultrasound Technology
Health Sciences > Radiology, Nuclear Medicine and Imaging
Life Sciences > Neurology
Health Sciences > Neurology (clinical)
Uncontrolled Keywords:Anatomy, Radiological and Ultrasound Technology, Radiology Nuclear Medicine and imaging, Neurology, Clinical Neurology, associative learning; discriminative fear conditioning; emotional learning; multivariate pattern analysis; spectrotemporal information; threat conditioning; threat representation
Language:English
Date:1 March 2020
Deposited On:24 Feb 2020 15:55
Last Modified:01 Aug 2020 18:35
Publisher:Wiley-Blackwell Publishing, Inc.
ISSN:1065-9471
OA Status:Hybrid
Free access at:PubMed ID. An embargo period may apply.
Publisher DOI:https://doi.org/10.1002/hbm.24846
PubMed ID:31663229

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