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      Thermosensory Perceptual Learning Is Associated with Structural Brain Changes in Parietal–Opercular (SII) Cortex

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          Abstract

          The location of a sensory cortex for temperature perception remains a topic of substantial debate. Both the parietal–opercular (SII) and posterior insula have been consistently implicated in thermosensory processing, but neither region has yet been identified as the locus of fine temperature discrimination. Using a perceptual learning paradigm in male and female humans, we show improvement in discrimination accuracy for subdegree changes in both warmth and cool detection over 5 d of repetitive training. We found that increases in discriminative accuracy were specific to the temperature (cold or warm) being trained. Using structural imaging to look for plastic changes associated with perceptual learning, we identified symmetrical increases in gray matter volume in the SII cortex. Furthermore, we observed distinct, adjacent regions for cold and warm discrimination, with cold discrimination having a more anterior locus than warm. The results suggest that thermosensory discrimination is supported by functionally and anatomically distinct temperature-specific modules in the SII cortex.

          SIGNIFICANCE STATEMENT We provide behavioral and neuroanatomical evidence that perceptual learning is possible within the temperature system. We show that structural plasticity localizes to parietal–opercular (SII), and not posterior insula, providing the best evidence to date resolving a longstanding debate about the location of putative “temperature cortex.” Furthermore, we show that cold and warm pathways are behaviorally and anatomically dissociable, suggesting that the temperature system has distinct temperature-dependent processing modules.

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          Most cited references36

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          The menthol receptor TRPM8 is the principal detector of environmental cold.

          Sensory nerve fibres can detect changes in temperature over a remarkably wide range, a process that has been proposed to involve direct activation of thermosensitive excitatory transient receptor potential (TRP) ion channels. One such channel--TRP melastatin 8 (TRPM8) or cold and menthol receptor 1 (CMR1)--is activated by chemical cooling agents (such as menthol) or when ambient temperatures drop below approximately 26 degrees C, suggesting that it mediates the detection of cold thermal stimuli by primary afferent sensory neurons. However, some studies have questioned the contribution of TRPM8 to cold detection or proposed that other excitatory or inhibitory channels are more critical to this sensory modality in vivo. Here we show that cultured sensory neurons and intact sensory nerve fibres from TRPM8-deficient mice exhibit profoundly diminished responses to cold. These animals also show clear behavioural deficits in their ability to discriminate between cold and warm surfaces, or to respond to evaporative cooling. At the same time, TRPM8 mutant mice are not completely insensitive to cold as they avoid contact with surfaces below 10 degrees C, albeit with reduced efficiency. Thus, our findings demonstrate an essential and predominant role for TRPM8 in thermosensation over a wide range of cold temperatures, validating the hypothesis that TRP channels are the principal sensors of thermal stimuli in the peripheral nervous system.
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            Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space.

            In both diagnostic and research applications, the interpretation of MR images of the human brain is facilitated when different data sets can be compared by visual inspection of equivalent anatomical planes. Quantitative analysis with predefined atlas templates often requires the initial alignment of atlas and image planes. Unfortunately, the axial planes acquired during separate scanning sessions are often different in their relative position and orientation, and these slices are not coplanar with those in the atlas. We have developed a completely automatic method to register a given volumetric data set with Talairach stereotaxic coordinate system. The registration method is based on multi-scale, three-dimensional (3D) cross-correlation with an average (n > 300) MR brain image volume aligned with the Talariach stereotaxic space. Once the data set is re-sampled by the transformation recovered by the algorithm, atlas slices can be directly superimposed on the corresponding slices of the re-sampled volume. the use of such a standardized space also allows the direct comparison, voxel to voxel, of two or more data sets brought into stereotaxic space. With use of a two-tailed Student t test for paired samples, there was no significant difference in the transformation parameters recovered by the automatic algorithm when compared with two manual landmark-based methods (p > 0.1 for all parameters except y-scale, where p > 0.05). Using root-mean-square difference between normalized voxel intensities as an unbiased measure of registration, we show that when estimated and averaged over 60 volumetric MR images in standard space, this measure was 30% lower for the automatic technique than the manual method, indicating better registrations. Likewise, the automatic method showed a 57% reduction in standard deviation, implying a more stable technique. The algorithm is able to recover the transformation even when data are missing from the top or bottom of the volume. We present a fully automatic registration method to map volumetric data into stereotaxic space that yields results comparable with those of manually based techniques. The method requires no manual identification of points or contours and therefore does not suffer the drawbacks involved in user intervention such as reproducibility and interobserver variability.
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              Significance of the insula for the evolution of human awareness of feelings from the body.

              An ascending sensory pathway that underlies feelings from the body, such as cooling or toothache, terminates in the posterior insula. Considerable evidence suggests that this activity is rerepresented and integrated first in the mid-insula and then in the anterior insula. Activation in the anterior insula correlates directly with subjective feelings from the body and, strikingly, with all emotional feelings. These findings appear to signify a posterior-to-anterior sequence of increasingly homeostatically efficient representations that integrate all salient neural activity, culminating in network nodes in the right and left anterior insulae that may be organized asymmetrically in an opponent fashion. The anterior insula has appropriate characteristics to support the proposal that it engenders a cinemascopic model of human awareness and subjectivity. This review presents the author's views regarding the principles of organization of this system and discusses a possible sequence for its evolution, as well as particular issues of historical interest. © 2011 New York Academy of Sciences.
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                Author and article information

                Journal
                J Neurosci
                J. Neurosci
                jneuro
                jneurosci
                J. Neurosci
                The Journal of Neuroscience
                Society for Neuroscience
                0270-6474
                1529-2401
                27 September 2017
                27 September 2017
                : 37
                : 39
                : 9380-9388
                Affiliations
                [1] 1Center for Information and Neural Networks, National Institute of Information and Communications Technology, Osaka, Japan 565-0871,
                [2] 2Advanced Telecommunications Research Institute International, Seika-cho, Soraku-gun, Kyoto 619-0288, Japan,
                [3] 3Graduate School of Environmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Aichi 464-0814, Japan,
                [4] 4Institute of Neurology, University College London, London WC1N 3BG, United Kingdom, and
                [5] 5Computational and Biological Learning Laboratory, Department of Engineering, University of Cambridge, Cambridge CB2 1PZ, United Kingdom
                Author notes
                Correspondence should be addressed to Ben Seymour, Computational and Biological Learning Laboratory, Department of Engineering, University of Cambridge, Trumpington Street, Cambridge CB2 1PZ, UK. bjs49@ 123456gmail.com

                Author contributions: H.M., W.Y., K.S., S.Z., M. Koltzenburg, M. Kawato, and B.S. designed research; H.M., W.Y., S.Z., and B.S. performed research; H.M. and B.S. analyzed data; H.M., W.Y., K.S., S.Z., M. Koltzenburg, M. Kawato, and B.S. wrote the paper.

                Author information
                http://orcid.org/0000-0001-9273-1617
                http://orcid.org/0000-0002-4183-3493
                http://orcid.org/0000-0001-9028-6265
                http://orcid.org/0000-0001-9181-5966
                http://orcid.org/0000-0003-1724-5832
                Article
                1316-17
                10.1523/JNEUROSCI.1316-17.2017
                5618259
                28847806
                d88cbdb1-de08-487e-a434-9af3eb958da1
                Copyright © 2017 Mano et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 14 May 2017
                : 30 June 2017
                : 31 July 2017
                Categories
                Research Articles
                Behavioral/Cognitive

                interoception,pain,perceptual learning,thermal,thermosensory,vbm

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