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      Sparse Codes for Speech Predict Spectrotemporal Receptive Fields in the Inferior Colliculus

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          Abstract

          We have developed a sparse mathematical representation of speech that minimizes the number of active model neurons needed to represent typical speech sounds. The model learns several well-known acoustic features of speech such as harmonic stacks, formants, onsets and terminations, but we also find more exotic structures in the spectrogram representation of sound such as localized checkerboard patterns and frequency-modulated excitatory subregions flanked by suppressive sidebands. Moreover, several of these novel features resemble neuronal receptive fields reported in the Inferior Colliculus (IC), as well as auditory thalamus and cortex, and our model neurons exhibit the same tradeoff in spectrotemporal resolution as has been observed in IC. To our knowledge, this is the first demonstration that receptive fields of neurons in the ascending mammalian auditory pathway beyond the auditory nerve can be predicted based on coding principles and the statistical properties of recorded sounds.

          Author Summary

          The receptive field of a neuron can be thought of as the stimulus that most strongly causes it to be active. Scientists have long been interested in discovering the underlying principles that determine the structure of receptive fields of cells in the auditory pathway to better understand how our brains process sound. One possible way of predicting these receptive fields is by using a theoretical model such as a sparse coding model. In such a model, each sound is represented by the smallest possible number of active model neurons chosen from a much larger group. A primary question addressed in this study is whether the receptive fields of model neurons optimized for natural sounds will predict receptive fields of actual neurons. Here, we use a sparse coding model on speech data. We find that our model neurons do predict receptive fields of auditory neurons, specifically in the Inferior Colliculus (midbrain) as well as the thalamus and cortex. To our knowledge, this is the first time any theoretical model has been able to predict so many of the diverse receptive fields of the various cell-types in those areas.

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          Most cited references37

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          Some informational aspects of visual perception.

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            Sparse coding and decorrelation in primary visual cortex during natural vision.

            Theoretical studies suggest that primary visual cortex (area V1) uses a sparse code to efficiently represent natural scenes. This issue was investigated by recording from V1 neurons in awake behaving macaques during both free viewing of natural scenes and conditions simulating natural vision. Stimulation of the nonclassical receptive field increases the selectivity and sparseness of individual V1 neurons, increases the sparseness of the population response distribution, and strongly decorrelates the responses of neuron pairs. These effects are due to both excitatory and suppressive modulation of the classical receptive field by the nonclassical receptive field and do not depend critically on the spatiotemporal structure of the stimuli. During natural vision, the classical and nonclassical receptive fields function together to form a sparse representation of the visual world. This sparse code may be computationally efficient for both early vision and higher visual processing.
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              Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex.

              We investigated the hypothesis that task performance can rapidly and adaptively reshape cortical receptive field properties in accord with specific task demands and salient sensory cues. We recorded neuronal responses in the primary auditory cortex of behaving ferrets that were trained to detect a target tone of any frequency. Cortical plasticity was quantified by measuring focal changes in each cell's spectrotemporal response field (STRF) in a series of passive and active behavioral conditions. STRF measurements were made simultaneously with task performance, providing multiple snapshots of the dynamic STRF during ongoing behavior. Attending to a specific target frequency during the detection task consistently induced localized facilitative changes in STRF shape, which were swift in onset. Such modulatory changes may enhance overall cortical responsiveness to the target tone and increase the likelihood of 'capturing' the attended target during the detection task. Some receptive field changes persisted for hours after the task was over and hence may contribute to long-term sensory memory.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS Comput Biol
                PLoS Comput. Biol
                plos
                ploscomp
                PLoS Computational Biology
                Public Library of Science (San Francisco, USA )
                1553-734X
                1553-7358
                July 2012
                July 2012
                12 July 2012
                : 8
                : 7
                : e1002594
                Affiliations
                [1 ]Redwood Center for Theoretical Neuroscience, University of California, Berkeley, California, United States of America
                [2 ]Department of Physics, University of California, Berkeley, California, United States of America
                [3 ]Helen Wills Neuroscience Institute, University of California, Berkeley, California, United States of America
                University of Oxford, United Kingdom
                Author notes

                Conceived and designed the experiments: NLC MRD. Performed the experiments: NLC. Analyzed the data: NLC VLM MRD. Wrote the paper: NLC MRD.

                Article
                PCOMPBIOL-D-11-01709
                10.1371/journal.pcbi.1002594
                3395612
                22807665
                17d33803-6774-411d-97bb-a12bcba89620
                Carlson et al. 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
                : 16 November 2011
                : 18 May 2012
                Page count
                Pages: 15
                Categories
                Research Article
                Biology
                Neuroscience
                Computational Neuroscience
                Coding Mechanisms
                Sensory Systems
                Sensory Systems
                Auditory System

                Quantitative & Systems biology
                Quantitative & Systems biology

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