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Mapping the tonotopic organization in human auditory cortex with minimally salient acoustic stimulation.

ABSTRACT: Despite numerous neuroimaging studies, the tonotopic organization in human auditory cortex is not yet unambiguously established. In this functional magnetic resonance imaging study, 20 subjects were presented with low-level task-irrelevant tones to avoid spread of cortical activation. Data-driven analyses were employed to obtain robust tonotopic maps. Two high-frequency endpoints were situated on the caudal and rostral banks of medial Heschl's gyrus, while low-frequency activation peaked on its lateral crest. Based on cortical parcellations, these 2 tonotopic progressions coincide with the primary auditory field (A1) in lateral koniocortex (Kl) and the rostral field (R) in medial koniocortex (Km), which together constitute a core region. Another gradient was found on the planum temporale. Our results show the bilateral existence of 3 tonotopic gradients in angulated orientations, which contrasts with colinear configurations that were suggested before. We argue that our results corroborate and elucidate the apparently contradictory findings in literature.

SUBMITTER: Langers DR

PROVIDER: S-EPMC3412441 | biostudies-literature | 2012 Sep

REPOSITORIES: biostudies-literature

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Mapping the tonotopic organization in human auditory cortex with minimally salient acoustic stimulation.

Langers Dave R M DR van Dijk Pim P

Cerebral cortex (New York, N.Y. : 1991) 20111006 9

Despite numerous neuroimaging studies, the tonotopic organization in human auditory cortex is not yet unambiguously established. In this functional magnetic resonance imaging study, 20 subjects were presented with low-level task-irrelevant tones to avoid spread of cortical activation. Data-driven analyses were employed to obtain robust tonotopic maps. Two high-frequency endpoints were situated on the caudal and rostral banks of medial Heschl's gyrus, while low-frequency activation peaked on its ...[more]

PMID: 21980020

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Project description:BackgroundWhile human auditory cortex is known to contain tonotopically organized auditory cortical fields (ACFs), little is known about how processing in these fields is modulated by other acoustic features or by attention.Methodology/principal findingsWe used functional magnetic resonance imaging (fMRI) and population-based cortical surface analysis to characterize the tonotopic organization of human auditory cortex and analyze the influence of tone intensity, ear of delivery, scanner background noise, and intermodal selective attention on auditory cortex activations. Medial auditory cortex surrounding Heschl's gyrus showed large sensory (unattended) activations with two mirror-symmetric tonotopic fields similar to those observed in non-human primates. Sensory responses in medial regions had symmetrical distributions with respect to the left and right hemispheres, were enlarged for tones of increased intensity, and were enhanced when sparse image acquisition reduced scanner acoustic noise. Spatial distribution analysis suggested that changes in tone intensity shifted activation within isofrequency bands. Activations to monaural tones were enhanced over the hemisphere contralateral to stimulation, where they produced activations similar to those produced by binaural sounds. Lateral regions of auditory cortex showed small sensory responses that were larger in the right than left hemisphere, lacked tonotopic organization, and were uninfluenced by acoustic parameters. Sensory responses in both medial and lateral auditory cortex decreased in magnitude throughout stimulus blocks. Attention-related modulations (ARMs) were larger in lateral than medial regions of auditory cortex and appeared to arise primarily in belt and parabelt auditory fields. ARMs lacked tonotopic organization, were unaffected by acoustic parameters, and had distributions that were distinct from those of sensory responses. Unlike the gradual adaptation seen for sensory responses, ARMs increased in amplitude throughout stimulus blocks.Conclusions/significanceThe results are consistent with the view that medial regions of human auditory cortex contain tonotopically organized core and belt fields that map the basic acoustic features of sounds while surrounding higher-order parabelt regions are tuned to more abstract stimulus attributes. Intermodal selective attention enhances processing in neuronal populations that are partially distinct from those activated by unattended stimuli.

Project description:Tonotopy is a fundamental organizational feature of the auditory system. Sounds are encoded by the spatial and temporal patterns of electrical activity in spiral ganglion neurons (SGNs) and are transmitted via tonotopically ordered processes from the cochlea through the eighth nerve to the cochlear nuclei. Upon reaching the brainstem, SGN axons bifurcate in a stereotyped pattern, innervating target neurons in the anteroventral cochlear nucleus (aVCN) with one branch and in the posteroventral and dorsal cochlear nuclei (pVCN and DCN) with the other. Each branch is tonotopically organized, thereby distributing acoustic information systematically along multiple parallel pathways for processing in the brainstem. In mice with a mutation in the receptor guanylyl cyclase Npr2, this spatial organization is disrupted. Peripheral SGN processes appear normal, but central SGN processes fail to bifurcate and are disorganized as they exit the auditory nerve. Within the cochlear nuclei, the tonotopic organization of the SGN terminal arbors is blurred and the aVCN is underinnervated with a reduced convergence of SGN inputs onto target neurons. The tonotopy of circuitry within the cochlear nuclei is also degraded, as revealed by changes in the topographic mapping of tuberculoventral cell projections from DCN to VCN. Nonetheless, Npr2 mutant SGN axons are able to transmit acoustic information with normal sensitivity and timing, as revealed by auditory brainstem responses and electrophysiological recordings from VCN neurons. Although most features of signal transmission are normal, intermittent failures were observed in responses to trains of shocks, likely due to a failure in action potential conduction at branch points in Npr2 mutant afferent fibers. Our results show that Npr2 is necessary for the precise spatial organization typical of central auditory circuits, but that signals are still transmitted with normal timing, and that mutant mice can hear even with these deficits.

Project description:Cortical information processing of the onset, offset, and continuous plateau of an acoustic stimulus should play an important role in acoustic object perception. To date, transient activities responding to the onset and offset of a sound have been well investigated and cortical subfields and topographic representation in these subfields, such as place code of sound frequency, have been well characterized. However, whether these cortical subfields with tonotopic representation are inherited in the sustained activities that follow transient activities and persist during the presentation of a long-lasting stimulus remains unknown, because sustained activities do not exhibit distinct, reproducible, and time-locked responses in their amplitude to be characterized by grand averaging. To address this gap in understanding, we attempted to decode sound information from densely mapped sustained activities in the rat auditory cortex using a sparse parameter estimation method called sparse logistic regression (SLR), and investigated whether and how these activities represent sound information. A microelectrode array with a grid of 10 × 10 recording sites within an area of 4.0 mm × 4.0 mm was implanted in the fourth layer of the auditory cortex in rats under isoflurane anesthesia. Sustained activities in response to long-lasting constant pure tones were recorded. SLR then was applied to discriminate the sound-induced band-specific power or phase-locking value from those of spontaneous activities. The highest decoding performance was achieved in the high-gamma band, indicating that cortical inhibitory interneurons may contribute to the sparse tonotopic representation in sustained activities by mediating synchronous activities. The estimated parameter in the SLR decoding revealed that the informative recording site had a characteristic frequency close to the test frequency. In addition, decoding of the four test frequencies demonstrated that the decoding performance of the SLR deteriorated when the test frequencies were close, supporting the hypothesis that the sustained activities were organized in a tonotopic manner. Finally, unlike transient activities, sustained activities were more informative in the belt than in the core region, indicating that higher-order auditory areas predominate over lower-order areas during sustained activities. Taken together, our results indicate that the auditory cortex processes sound information tonotopically and in a hierarchical manner.

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Mapping the tonotopic organization in human auditory cortex with minimally salient acoustic stimulation.

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Mapping the tonotopic organization in human auditory cortex with minimally salient acoustic stimulation.

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