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      Selective Attention Modulates Human Auditory Brainstem Responses: Relative Contributions of Frequency and Spatial Cues

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      1 , 2 , 3 , 1 , 2 , 3 , 4 , *
      PLoS ONE
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          Abstract

          Selective attention is the mechanism that allows focusing one’s attention on a particular stimulus while filtering out a range of other stimuli, for instance, on a single conversation in a noisy room. Attending to one sound source rather than another changes activity in the human auditory cortex, but it is unclear whether attention to different acoustic features, such as voice pitch and speaker location, modulates subcortical activity. Studies using a dichotic listening paradigm indicated that auditory brainstem processing may be modulated by the direction of attention. We investigated whether endogenous selective attention to one of two speech signals affects amplitude and phase locking in auditory brainstem responses when the signals were either discriminable by frequency content alone, or by frequency content and spatial location. Frequency-following responses to the speech sounds were significantly modulated in both conditions. The modulation was specific to the task-relevant frequency band. The effect was stronger when both frequency and spatial information were available. Patterns of response were variable between participants, and were correlated with psychophysical discriminability of the stimuli, suggesting that the modulation was biologically relevant. Our results demonstrate that auditory brainstem responses are susceptible to efferent modulation related to behavioral goals. Furthermore they suggest that mechanisms of selective attention actively shape activity at early subcortical processing stages according to task relevance and based on frequency and spatial cues.

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          Most cited references26

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          Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence.

          Both physiological and behavioral studies have suggested that stimulus-driven neural activity in the sensory pathways can be modulated in amplitude during selective attention. Recordings of event-related brain potentials indicate that such sensory gain control or amplification processes play an important role in visual-spatial attention. Combined event-related brain potential and neuroimaging experiments provide strong evidence that attentional gain control operates at an early stage of visual processing in extrastriate cortical areas. These data support early selection theories of attention and provide a basis for distinguishing between separate mechanisms of attentional suppression (of unattended inputs) and attentional facilitation (of attended inputs).
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            Modulation of early sensory processing in human auditory cortex during auditory selective attention.

            Neuromagnetic fields were recorded from human subjects as they listened selectively to sequences of rapidly presented tones in one ear while ignoring tones of a different pitch in the opposite ear. Tones in the attended ear evoked larger magnetic brain responses than did unattended tones in the latency ranges 20-50 msec and 80-130 msec poststimulus. Source localization techniques in conjunction with magnetic resonance imaging placed the neural generators of these early attention-sensitive brain responses in auditory cortex on the supratemporal plane. These data demonstrate that focused auditory attention in humans can selectively modulate sensory processing in auditory cortex beginning as early as 20 msec poststimulus, thereby providing strong evidence for an "early selection" mechanism of auditory attention that can regulate auditory input at or before the initial stages of cortical analysis.
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              Cross-domain effects of music and language experience on the representation of pitch in the human auditory brainstem.

              Neural encoding of pitch in the auditory brainstem is known to be shaped by long-term experience with language or music, implying that early sensory processing is subject to experience-dependent neural plasticity. In language, pitch patterns consist of sequences of continuous, curvilinear contours; in music, pitch patterns consist of relatively discrete, stair-stepped sequences of notes. The primary aim was to determine the influence of domain-specific experience (language vs. music) on the encoding of pitch in the brainstem. Frequency-following responses were recorded from the brainstem in native Chinese, English amateur musicians, and English nonmusicians in response to iterated rippled noise homologues of a musical pitch interval (major third; M3) and a lexical tone (Mandarin tone 2; T2) from the music and language domains, respectively. Pitch-tracking accuracy (whole contour) and pitch strength (50 msec sections) were computed from the brainstem responses using autocorrelation algorithms. Pitch-tracking accuracy was higher in the Chinese and musicians than in the nonmusicians across domains. Pitch strength was more robust across sections in musicians than in nonmusicians regardless of domain. In contrast, the Chinese showed larger pitch strength, relative to nonmusicians, only in those sections of T2 with rapid changes in pitch. Interestingly, musicians exhibited greater pitch strength than the Chinese in one section of M3, corresponding to the onset of the second musical note, and two sections within T2, corresponding to a note along the diatonic musical scale. We infer that experience-dependent plasticity of brainstem responses is shaped by the relative saliency of acoustic dimensions underlying the pitch patterns associated with a particular domain.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                15 January 2014
                : 9
                : 1
                : e85442
                Affiliations
                [1 ]Laboratory for Brain, Music and Sound Research (BRAMS), Montreal, Canada
                [2 ]Department of Psychology, University of Montreal, Montreal, Canada
                [3 ]Centre for Research on Brain, Language and Music (CRBLM), Montreal, Canada
                [4 ]Montreal Neurological Institute, McGill University, Montreal, Canada
                Harvard Medical School/Massachusetts General Hospital, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AL MS. Performed the experiments: AL. Analyzed the data: AL. Contributed reagents/materials/analysis tools: MS. Wrote the paper: AL MS.

                Article
                PONE-D-13-24756
                10.1371/journal.pone.0085442
                3893196
                24454869
                5c368487-d60d-471d-a8a5-da347f7ab722
                Copyright @ 2014

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 13 June 2013
                : 27 November 2013
                Page count
                Pages: 10
                Funding
                This work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC, www.nserc-crsng.gc.ca) grant, #365345, to MS and a post-doctoral research grant from the Department of Foreign Affairs and International Trade Canada to AL. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Neuroscience
                Cognitive Neuroscience
                Cognition
                Sensory Perception
                Psychoacoustics
                Sensory Systems
                Auditory System
                Medicine
                Mental Health
                Psychology
                Behavior
                Attention (Behavior)
                Cognitive Psychology
                Experimental Psychology
                Social and Behavioral Sciences
                Psychology
                Behavior
                Attention (Behavior)
                Cognitive Psychology
                Experimental Psychology

                Uncategorized
                Uncategorized

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