Representation of the temporal envelope of sounds in the human brain

Citation
Al. Giraud et al., Representation of the temporal envelope of sounds in the human brain, J NEUROPHYS, 84(3), 2000, pp. 1588-1598
Citations number
55
Categorie Soggetti
Neurosciences & Behavoir
Journal title
JOURNAL OF NEUROPHYSIOLOGY
ISSN journal
00223077 → ACNP
Volume
84
Issue
3
Year of publication
2000
Pages
1588 - 1598
Database
ISI
SICI code
0022-3077(200009)84:3<1588:ROTTEO>2.0.ZU;2-9
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 frequen cies ranging from 4 to 256 Hz. This range includes low AM frequencies (up t o 32 Hz) essential for the perception of the manner of articulation and syl labic rate, and high AM frequencies (above 64 Hz) essential for the percept ion of voicing and prosody. The right lower brainstem (superior olivary com plex), the right inferior colliculus, the left medial geniculate body, Hesc hl's gyrus, the superior temporal gyrus, the superior temporal sulcus, and the inferior parietal lobule were specifically responsive to AM. Global tun ing curves in these regions suggest that the human auditory system is organ ized as a hierarchical filter bank, each processing level responding prefer entially 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 fo r the primary auditory cortex, and 4-8 Hz for secondary regions. The time c ourse of the hemodynamic responses showed sustained and transient component s with reverse frequency dependent patterns: the lower the AM frequency the better the fit with a sustained response model, the higher the AM frequenc y the better the fit with a transient response model. Using cortical maps o f best modulation frequency, we demonstrate that the spatial representation of AM frequencies varies according to the response type. Sustained respons es yield maps of low frequencies organized in large clusters. Transient res ponses yield maps of high frequencies represented by a mosaic of small clus ters. Very few voxels were tuned to intermediate frequencies (32-64 Hz). We did not find spatial gradients of AM frequencies associated with any respo nse type. Our results suggest that two frequency ranges (up to 16 and 128 H z and above) are represented in the cortex by different response types. How ever, the spatial segregation of these two ranges is not systematic. Most c ortical regions were tuned to low frequencies and only a few to high freque ncies. Yet, voxels that show a preference for low frequencies were also res ponsive to high frequencies. Overall, our study shows that the temporal env elope of sounds is processed by both distinct (hierarchically organized ser ies of filters) and shared (high and low AM frequencies eliciting different responses at the same cortical locus) neural substrates. This layout sugge sts 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 comple mentary features in cortical auditory regions.