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      High-Field Functional Imaging of Pitch Processing in Auditory Cortex of the Cat

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          Abstract

          The perception of pitch is a widely studied and hotly debated topic in human hearing. Many of these studies combine functional imaging techniques with stimuli designed to disambiguate the percept of pitch from frequency information present in the stimulus. While useful in identifying potential “pitch centres” in cortex, the existence of truly pitch-responsive neurons requires single neuron-level measures that can only be undertaken in animal models. While a number of animals have been shown to be sensitive to pitch, few studies have addressed the location of cortical generators of pitch percepts in non-human models. The current study uses high-field functional magnetic resonance imaging (fMRI) of the feline brain in an attempt to identify regions of cortex that show increased activity in response to pitch-evoking stimuli. Cats were presented with iterated rippled noise (IRN) stimuli, narrowband noise stimuli with the same spectral profile but no perceivable pitch, and a processed IRN stimulus in which phase components were randomized to preserve slowly changing modulations in the absence of pitch (IRNo). Pitch-related activity was not observed to occur in either primary auditory cortex (A1) or the anterior auditory field (AAF) which comprise the core auditory cortex in cats. Rather, cortical areas surrounding the posterior ectosylvian sulcus responded preferentially to the IRN stimulus when compared to narrowband noise, with group analyses revealing bilateral activity centred in the posterior auditory field (PAF). This study demonstrates that fMRI is useful for identifying pitch-related processing in cat cortex, and identifies cortical areas that warrant further investigation. Moreover, we have taken the first steps in identifying a useful animal model for the study of pitch perception.

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          Most cited references29

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          Sound localization by human listeners.

          In keeping with our promise earlier in this review, we summarize here the process by which we believe spatial cues are used for localizing a sound source in a free-field listening situation. We believe it entails two parallel processes: 1. The azimuth of the source is determined using differences in interaural time or interaural intensity, whichever is present. Wightman and colleagues (1989) believe the low-frequency temporal information is dominant if both are present. 2. The elevation of the source is determined from spectral shape cues. The received sound spectrum, as modified by the pinna, is in effect compared with a stored set of directional transfer functions. These are actually the spectra of a nearly flat source heard at various elevations. The elevation that corresponds to the best-matching transfer function is selected as the locus of the sound. Pinnae are similar enough between people that certain general rules (e.g. Blauert's boosted bands or Butler's covert peaks) can describe this process. Head motion is probably not a critical part of the localization process, except in cases where time permits a very detailed assessment of location, in which case one tries to localize the source by turning the head toward the putative location. Sound localization is only moderately more precise when the listener points directly toward the source. The process is not analogous to localizing a visual source on the fovea of the retina. Thus, head motion provides only a moderate increase in localization accuracy. Finally, current evidence does not support the view that auditory motion perception is anything more than detection of changes in static location over time.
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            The processing of temporal pitch and melody information in auditory cortex.

            An fMRI experiment was performed to identify the main stages of melody processing in the auditory pathway. Spectrally matched sounds that produce no pitch, fixed pitch, or melody were all found to activate Heschl's gyrus (HG) and planum temporale (PT). Within this region, sounds with pitch produced more activation than those without pitch only in the lateral half of HG. When the pitch was varied to produce a melody, there was activation in regions beyond HG and PT, specifically in the superior temporal gyrus (STG) and planum polare (PP). The results support the view that there is hierarchy of pitch processing in which the center of activity moves anterolaterally away from primary auditory cortex as the processing of melodic sounds proceeds.
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              The neuronal representation of pitch in primate auditory cortex.

              Pitch perception is critical for identifying and segregating auditory objects, especially in the context of music and speech. The perception of pitch is not unique to humans and has been experimentally demonstrated in several animal species. Pitch is the subjective attribute of a sound's fundamental frequency (f(0)) that is determined by both the temporal regularity and average repetition rate of its acoustic waveform. Spectrally dissimilar sounds can have the same pitch if they share a common f(0). Even when the acoustic energy at f(0) is removed ('missing fundamental') the same pitch is still perceived. Despite its importance for hearing, how pitch is represented in the cerebral cortex is unknown. Here we show the existence of neurons in the auditory cortex of marmoset monkeys that respond to both pure tones and missing fundamental harmonic complex sounds with the same f(0), providing a neural correlate for pitch constancy. These pitch-selective neurons are located in a restricted low-frequency cortical region near the anterolateral border of the primary auditory cortex, and is consistent with the location of a pitch-selective area identified in recent imaging studies in humans.
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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, CA USA )
                1932-6203
                30 July 2015
                2015
                : 10
                : 7
                : e0134362
                Affiliations
                [1 ]Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario, Canada
                [2 ]Brain and Mind Institute, University of Western Ontario, London, Ontario, Canada
                [3 ]Department of Anatomy and Cell Biology, University of Western Ontario, London, Ontario, Canada
                [4 ]Department of Psychology, University of Western Ontario, London, Ontario, Canada
                [5 ]National Centre for Audiology, University of Western Ontario, London, Ontario, Canada
                Kyoto University, JAPAN
                Author notes

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

                Conceived and designed the experiments: BEB AJH SGL. Performed the experiments: BEB AJH. Analyzed the data: BEB. Wrote the paper: BEB AJH SGL.

                Article
                PONE-D-15-03261
                10.1371/journal.pone.0134362
                4520558
                26225563
                9eec6b83-c4bd-41d7-b306-c92ddcaa928e
                Copyright @ 2015

                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
                : 22 January 2015
                : 9 July 2015
                Page count
                Figures: 5, Tables: 0, Pages: 13
                Funding
                Funding for this project was provided by the Natural Sciences and Engineering Research Council, the Canadian Institutes for Health Research, and the Canada Foundation for Innovation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
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                All relevant data are within the paper.

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