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      Diminished Behavioral and Neural Sensitivity to Sound Modulation Is Associated with Moderate Developmental Hearing Loss

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          Abstract

          The acoustic rearing environment can alter central auditory coding properties, yet altered neural coding is seldom linked with specific deficits to adult perceptual skills. To test whether developmental hearing loss resulted in comparable changes to perception and sensory coding, we examined behavioral and neural detection thresholds for sinusoidally amplitude modulated (sAM) stimuli. Behavioral sAM detection thresholds for slow (5 Hz) modulations were significantly worse for animals reared with bilateral conductive hearing loss (CHL), as compared to controls. This difference could not be attributed to hearing thresholds, proficiency at the task, or proxies for attention. Detection thresholds across the groups did not differ for fast (100 Hz) modulations, a result paralleling that seen in humans. Neural responses to sAM stimuli were recorded in single auditory cortex neurons from separate groups of awake animals. Neurometric analyses indicated equivalent thresholds for the most sensitive neurons, but a significantly poorer detection threshold for slow modulations across the population of CHL neurons as compared to controls. The magnitude of the neural deficit matched that of the behavioral differences, suggesting that a reduction of sensory information can account for limitations to perceptual skills.

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          Most cited references77

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          The analysis of visual motion: a comparison of neuronal and psychophysical performance.

          We compared the ability of psychophysical observers and single cortical neurons to discriminate weak motion signals in a stochastic visual display. All data were obtained from rhesus monkeys trained to perform a direction discrimination task near psychophysical threshold. The conditions for such a comparison were ideal in that both psychophysical and physiological data were obtained in the same animals, on the same sets of trials, and using the same visual display. In addition, the psychophysical task was tailored in each experiment to the physiological properties of the neuron under study; the visual display was matched to each neuron's preference for size, speed, and direction of motion. Under these conditions, the sensitivity of most MT neurons was very similar to the psychophysical sensitivity of the animal observers. In fact, the responses of single neurons typically provided a satisfactory account of both absolute psychophysical threshold and the shape of the psychometric function relating performance to the strength of the motion signal. Thus, psychophysical decisions in our task are likely to be based upon a relatively small number of neural signals. These signals could be carried by a small number of neurons if the responses of the pooled neurons are statistically independent. Alternatively, the signals may be carried by a much larger pool of neurons if their responses are partially intercorrelated.
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            Speech recognition with primarily temporal cues.

            Nearly perfect speech recognition was observed under conditions of greatly reduced spectral information. Temporal envelopes of speech were extracted from broad frequency bands and were used to modulate noises of the same bandwidths. This manipulation preserved temporal envelope cues in each band but restricted the listener to severely degraded information on the distribution of spectral energy. The identification of consonants, vowels, and words in simple sentences improved markedly as the number of bands increased; high speech recognition performance was obtained with only three bands of modulated noise. Thus, the presentation of a dynamic temporal pattern in only a few broad spectral regions is sufficient for the recognition of speech.
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              Subdivisions of auditory cortex and processing streams in primates.

              The auditory system of monkeys includes a large number of interconnected subcortical nuclei and cortical areas. At subcortical levels, the structural components of the auditory system of monkeys resemble those of nonprimates, but the organization at cortical levels is different. In monkeys, the ventral nucleus of the medial geniculate complex projects in parallel to a core of three primary-like auditory areas, AI, R, and RT, constituting the first stage of cortical processing. These areas interconnect and project to the homotopic and other locations in the opposite cerebral hemisphere and to a surrounding array of eight proposed belt areas as a second stage of cortical processing. The belt areas in turn project in overlapping patterns to a lateral parabelt region with at least rostral and caudal subdivisions as a third stage of cortical processing. The divisions of the parabelt distribute to adjoining auditory and multimodal regions of the temporal lobe and to four functionally distinct regions of the frontal lobe. Histochemically, chimpanzees and humans have an auditory core that closely resembles that of monkeys. The challenge for future researchers is to understand how this complex system in monkeys analyzes and utilizes auditory information.
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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
                2012
                26 July 2012
                : 7
                : 7
                : e41514
                Affiliations
                [1 ]Department of Anatomy and Neurobiology, Northeast Ohio Medical University, Rootstown, Ohio, United States of America
                [2 ]Center for Neural Science, New York University, New York, New York, United States of America
                [3 ]Department of Biology, New York University, New York, New York, United States of America
                [4 ]Department of Psychology, Carleton University, Ottawa, Ontario, Canada
                University of Auckland, New Zealand
                Author notes

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

                Conceived and designed the experiments: MJR DHS. Performed the experiments: MJR ECS. Analyzed the data: MJR. Contributed reagents/materials/analysis tools: JBK DHS. Wrote the paper: MJR DHS. Designed the software used in analysis: MJR.

                Article
                PONE-D-11-08927
                10.1371/journal.pone.0041514
                3406049
                22848517
                b0c79646-958a-495e-b331-25d6446036c5
                Copyright @ 2012

                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
                : 5 March 2012
                : 22 June 2012
                Page count
                Pages: 13
                Funding
                This work was supported by National Institutes of Health DC009165 (MJR), National Organization for Hearing Research Foundation (MJR), National Institutes of Health DC009237 (DHS), and New York University Research Challenge Fund (DHS). 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
                Computational Neuroscience
                Coding Mechanisms
                Sensory Systems
                Single Neuron Function
                Developmental Neuroscience
                Synaptic Plasticity
                Neurophysiology
                Central Nervous System
                Sensory Perception
                Sensory Deprivation
                Sensory Systems
                Auditory System
                Behavioral Neuroscience
                Neuropsychology
                Medicine
                Otorhinolaryngology
                Otology
                Hearing Disorders

                Uncategorized
                Uncategorized

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