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      The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex

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          Abstract

          The fact that feed-forward and top-down propagation of sensory information use distinct frequency bands is an appealing assumption for which evidence remains scarce. Here we obtain human depth recordings from two auditory cortical regions in both hemispheres, while subjects listen to sentences, and show that information travels in each direction using separate frequency channels. Bottom-up and top-down propagation dominates in γ- and δβ (<40 Hz) bands, respectively. The predominance of low frequencies for top-down information transfer is confirmed by cross-regional frequency coupling, which indicates that the power of γ-activity in A1 is modulated by the phase of δβ activity sampled from association auditory cortex (AAC). This cross-regional coupling effect is absent in the opposite direction. Finally, we show that information transfer does not proceed continuously but by time windows where bottom-up or top-down processing alternatively dominates. These findings suggest that the brain uses both frequency- and time-division multiplexing to optimize directional information transfer.

          Abstract

          Sensory processing relies on information transfer in cortical hierarchies. Using depth recordings of neural activity obtained while individuals with epilepsy listen to spoken sentences, the authors show that ascending and descending information is propagated between cortical regions through distinct neural frequencies.

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          Most cited references32

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          High-frequency, long-range coupling between prefrontal and visual cortex during attention.

          Electrical recordings in humans and monkeys show attentional enhancement of evoked responses and gamma synchrony in ventral stream cortical areas. Does this synchrony result from intrinsic activity in visual cortex or from inputs from other structures? Using paired recordings in the frontal eye field (FEF) and area V4, we found that attention to a stimulus in their joint receptive field leads to enhanced oscillatory coupling between the two areas, particularly at gamma frequencies. This coupling appeared to be initiated by FEF and was time-shifted by about 8 to 13 milliseconds across a range of frequencies. Considering the expected conduction and synaptic delays between the areas, this time-shifted coupling at gamma frequencies may optimize the postsynaptic impact of spikes from one area upon the other, improving cross-area communication with attention.
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            Beta oscillations in a large-scale sensorimotor cortical network: directional influences revealed by Granger causality.

            Previous studies have shown that synchronized beta frequency (14-30 Hz) oscillations in the primary motor cortex are involved in maintaining steady contractions of contralateral arm and hand muscles. However, little is known about the role of postcentral cortical areas in motor maintenance and their patterns of interaction with motor cortex. We investigated the functional relations of beta-synchronized neuronal assemblies in pre- and postcentral areas of two monkeys as they pressed a hand lever during the wait period of a visual discrimination task. By using power and coherence spectral analysis, we identified a beta-synchronized large-scale network linking pre- and postcentral areas. We then used Granger causality spectra to measure directional influences among recording sites. In both monkeys, strong Granger causal influences were observed from primary somatosensory cortex to both motor cortex and inferior posterior parietal cortex, with the latter area also exerting Granger causal influences on motor cortex. Granger causal influences from motor cortex to postcentral sites, however, were weak in one monkey and not observed in the other. These results are the first, to our knowledge, to demonstrate in awake monkeys that synchronized beta oscillations bind multiple sensorimotor areas into a large-scale network during motor maintenance behavior and carry Granger causal influences from primary somatosensory and inferior posterior parietal cortices to motor cortex.
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              Cross-frequency phase-phase coupling between θ and γ oscillations in the hippocampus.

              Neuronal oscillations allow for temporal segmentation of neuronal spikes. Interdependent oscillators can integrate multiple layers of information. We examined phase-phase coupling of theta and gamma oscillators in the CA1 region of rat hippocampus during maze exploration and rapid eye movement sleep. Hippocampal theta waves were asymmetric, and estimation of the spatial position of the animal was improved by identifying the waveform-based phase of spiking, compared to traditional methods used for phase estimation. Using the waveform-based theta phase, three distinct gamma bands were identified: slow gamma(S) (gamma(S); 30-50 Hz), midfrequency gamma(M) (gamma(M); 50-90 Hz), and fast gamma(F) (gamma(F); 90-150 Hz or epsilon band). The amplitude of each sub-band was modulated by the theta phase. In addition, we found reliable phase-phase coupling between theta and both gamma(S) and gamma(M) but not gamma(F) oscillators. We suggest that cross-frequency phase coupling can support multiple time-scale control of neuronal spikes within and across structures.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                02 September 2014
                : 5
                : 4694
                Affiliations
                [1 ]Department of Neuroscience, University of Geneva , Biotech Campus, 9, Chemin des Mines, Geneva 1211, Switzerland
                [2 ]Department of Psychiatry, Columbia University Medical Center , New York, New York 10032, USA
                [3 ]INSERM U1106—Institut de Neurosciences des Systèmes, Université Aix-Marseille , Marseille 13005, France
                [4 ]These authors contributed equally to this work
                Author notes
                Article
                ncomms5694
                10.1038/ncomms5694
                4164774
                25178489
                094f09cf-f28b-4d9d-9f6a-bc38b9e1150f
                Copyright © 2014, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 19 May 2014
                : 14 July 2014
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