The Journal of Neurophysiology Vol. 84 No. 3 September 2000, pp. 1588-1598
Copyright ©2000 by the American Physiological Society
Representation of the Temporal Envelope of Sounds in the
Human Brain
Anne-Lise
Giraud,1,4,*
Christian
Lorenzi,2,*
John
Ashburner,1
Jocelyne
Wable,3
Ingrid
Johnsrude,1
Richard
Frackowiak,1 and
Andreas
Kleinschmidt1,4
1Wellcome Department of Cognitive Neurology,
Institute of Neurology, London WC1N 3BG, United Kingdom;
2Laboratoire de Psychologie Expérimentale,
Unité Mixte de Recherche, 8581 Centre National de la Recherche
Scientifique, Unité de Formation et de Recherche Institut de
Psychologie, Université Paris V, 75006 Paris;
3Service Otorhinolaryngology,
Hôpital Avicenne, 93009 Bobigny Cédex, France; and
4Johann Wolfgang Goethe University, 60590 Frankfurt, Germany
Giraud, Anne-Lise,
Christian Lorenzi,
John Ashburner,
Jocelyne Wable,
Ingrid Johnsrude,
Richard Frackowiak, and
Andreas Kleinschmidt.
Representation of the Temporal Envelope of Sounds in the
Human Brain. J. Neurophysiol. 84: 1588-1598, 2000. 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.
*
A.-L. Giraud and C. Lorenzi contributed equally to the study.
