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Cited by 353Neuroscience and Music PerceptionHearing, Cochlea, Tinnitus, GeneticsTactile and Sensory Interactions

Representation of the temporal envelope of sounds in the human brain

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Giraud, Anne-Lise, Lorenzi, Christian, Ashburner, John, Wable, Jocelyne, Johnsrude, Ingrid, Frackowiak, Richard, Kleinschmidt, Andreas·2000·Journal of Neurophysiology
DOI 10.1152/jn.2000.84.3.1588
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Abstract

The cerebral representation of the temporal envelope of sounds was studied in five normal-hearing subjects using functional magnetic resonance imaging. The stimuli were white noise, sinusoidally amplitude-modulated at frequencies ranging from 4 to 256 Hz. This range includes low AM frequencies (up to 32 Hz) essential for the perception of the manner of articulation and syllabic rate, and high AM frequencies (above 64 Hz) essential for the perception of voicing and prosody. The right lower brainstem (superior olivary complex), the right inferior colliculus, the left medial geniculate body, Heschl's gyrus, the superior temporal gyrus, the superior temporal sulcus, and the inferior parietal lobule were specifically responsive to AM. Global tuning curves in these regions suggest that the human auditory system is organized as a hierarchical filter bank, each processing level responding preferentially to a given AM frequency, 256 Hz for the lower brainstem, 32-256 Hz for the inferior colliculus, 16 Hz for the medial geniculate body, 8 Hz for the primary auditory cortex, and 4-8 Hz for secondary regions. The time course of the hemodynamic responses showed sustained and transient components with reverse frequency dependent patterns: the lower the AM frequency the better the fit with a sustained response model, the higher the AM frequency the better the fit with a transient response model. Using cortical maps of best modulation frequency, we demonstrate that the spatial representation of AM frequencies varies according to the response type. Sustained responses yield maps of low frequencies organized in large clusters. Transient responses yield maps of high frequencies represented by a mosaic of small clusters. Very few voxels were tuned to intermediate frequencies (32-64 Hz). We did not find spatial gradients of AM frequencies associated with any response type. Our results suggest that two frequency ranges (up to 16 and 128 Hz and above) are represented in the cortex by different response types. However, the spatial segregation of these two ranges is not systematic. Most cortical regions were tuned to low frequencies and only a few to high frequencies. Yet, voxels that show a preference for low frequencies were also responsive to high frequencies. Overall, our study shows that the temporal envelope of sounds is processed by both distinct (hierarchically organized series of filters) and shared (high and low AM frequencies eliciting different responses at the same cortical locus) neural substrates. This layout suggests that the human auditory system is organized in a parallel fashion that allows a degree of separate routing for groups of AM frequencies conveying different information and preserves a possibility for integration of complementary features in cortical auditory regions.

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  • Left lateralized responses to nonspeech sounds in the auditory cortex are associated with rapid relative to slow frequency transitions.

    “Left lateralized responses to nonspeech sounds were identified in the auditory cortex (superior temporal gyri) by Belin et al. (1998) when participants listened to nonverbal sounds containing rapid relative to slow frequency transitions (Belin et al., 1998; Zatorre and Belin, 2001; Giraud et al., 2000).”

    From A review and synthesis of the first 20years of PET and fMRI studies of heard speech, spoken language and reading (2012) · cites this paper as Giraud et al., 2000

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Authors
Giraud, A.-L., Lorenzi, C., Ashburner, J., Wable, J., Johnsrude, I., Frackowiak, R., & Kleinschmidt, A.
Affiliations
  • Goethe University Frankfurt (DE)
  • Centre National de la Recherche Scientifique (FR)
  • UCL Queen Square Institute of Neurology (GB)
  • Hôpital Avicenne (FR)
ORCID
Venue
Journal of Neurophysiology
Publisher
American Physiological Society
Published
2000-09-01
Volume
84
Issue
3
Pages
1588-1598
ISSN
  • 0022-3077 (ISSN-L)
  • 1522-1598
DOI
10.1152/jn.2000.84.3.1588
OpenAlex
W1838748884
Cited by
353
References
53
Citations by year
2026: 1 · 2025: 8 · 2024: 10 · 2023: 10 · 2022: 14 · 2021: 9 · 2020: 19 · 2019: 21 · 2018: 13 · 2017: 13 · 2016: 14 · 2015: 19 · 2014: 10 · 2013: 19 · 2012: 22
FWCI
6.62
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Journal of Neurophysiology (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • UCL Discovery (University College London) (submittedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neuroscience and Music Perception
  • Life Sciences › Neuroscience › Sensory Systems › Hearing, Cochlea, Tinnitus, Genetics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
Keywords
temporal envelope, amplitude modulation, auditory cortex, auditory pathway, superior olivary complex, inferior colliculus, medial geniculate body, primary auditory cortex, superior temporal gyrus, inferior parietal lobule, hemodynamic response, auditory temporal processing, prosody, voicing perception
MeSH terms
Acoustic Stimulation, Adult, Brain, Brain Mapping, Female, Humans, Magnetic Resonance Imaging, Male, Models, Neurological, Pitch Perception, Reaction Time, Sound, Speech Perception, Evoked Potentials, Auditory, Brain Stem

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