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      Predictive Dynamics of Human Pain Perception

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          Abstract

          While the static magnitude of thermal pain perception has been shown to follow a power-law function of the temperature, its dynamical features have been largely overlooked. Due to the slow temporal experience of pain, multiple studies now show that the time evolution of its magnitude can be captured with continuous online ratings. Here we use such ratings to model quantitatively the temporal dynamics of thermal pain perception. We show that a differential equation captures the details of the temporal evolution in pain ratings in individual subjects for different stimulus pattern complexities, and also demonstrates strong predictive power to infer pain ratings, including readouts based only on brain functional images.

          Author Summary

          We propose a model of thermal pain perception that accounts for its dynamical behavior, and can be used to predict subjective responses to thermal stimulation on individual subjects with high accuracy, close to 90% averaged over subjects (over 65% for the null hypothesis). The model is based on behavioral considerations that include the need to signal current or approaching tissue damage, and the need to discount past danger. Moreover, we show that in a ‘mind reading’ setting, the combined use of sparse regression to infer pain perception from functional MRI recordings (fMRI), and from the model applied to the stimulus temperature also inferred from fMRI, leads to equally significant predictive accuracy, close to 75% averaged over subjects. Our results demonstrate that a subjective percept such as pain displays a highly deterministic behavior.

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          Most cited references15

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          Identifying natural images from human brain activity.

          A challenging goal in neuroscience is to be able to read out, or decode, mental content from brain activity. Recent functional magnetic resonance imaging (fMRI) studies have decoded orientation, position and object category from activity in visual cortex. However, these studies typically used relatively simple stimuli (for example, gratings) or images drawn from fixed categories (for example, faces, houses), and decoding was based on previous measurements of brain activity evoked by those same stimuli or categories. To overcome these limitations, here we develop a decoding method based on quantitative receptive-field models that characterize the relationship between visual stimuli and fMRI activity in early visual areas. These models describe the tuning of individual voxels for space, orientation and spatial frequency, and are estimated directly from responses evoked by natural images. We show that these receptive-field models make it possible to identify, from a large set of completely novel natural images, which specific image was seen by an observer. Identification is not a mere consequence of the retinotopic organization of visual areas; simpler receptive-field models that describe only spatial tuning yield much poorer identification performance. Our results suggest that it may soon be possible to reconstruct a picture of a person's visual experience from measurements of brain activity alone.
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            Predicting human brain activity associated with the meanings of nouns.

            The question of how the human brain represents conceptual knowledge has been debated in many scientific fields. Brain imaging studies have shown that different spatial patterns of neural activation are associated with thinking about different semantic categories of pictures and words (for example, tools, buildings, and animals). We present a computational model that predicts the functional magnetic resonance imaging (fMRI) neural activation associated with words for which fMRI data are not yet available. This model is trained with a combination of data from a trillion-word text corpus and observed fMRI data associated with viewing several dozen concrete nouns. Once trained, the model predicts fMRI activation for thousands of other concrete nouns in the text corpus, with highly significant accuracies over the 60 nouns for which we currently have fMRI data.
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              Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition.

              The temporal features of tactile stimuli are faithfully represented by the activity of neurons in the somatosensory cortex. However, the cellular mechanisms that enable cortical neurons to report accurate temporal information are not known. Here, we show that in the rodent barrel cortex, the temporal window for integration of thalamic inputs is under the control of thalamocortical feed-forward inhibition and can vary from 1 to 10 ms. A single thalamic fiber can trigger feed-forward inhibition and contacts both excitatory and inhibitory cortical neurons. The dynamics of feed-forward inhibition exceed those of each individual synapse in the circuit and are captured by a simple disynaptic model of the thalamocortical projection. The variations in the integration window produce changes in the temporal precision of cortical responses to whisker stimulation. Hence, feed-forward inhibitory circuits, classically known to sharpen spatial contrast of tactile inputs, also increase the temporal resolution in the somatosensory cortex.
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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
                October 2012
                October 2012
                25 October 2012
                : 8
                : 10
                : e1002719
                Affiliations
                [1 ]Computational Biology Center, T.J. Watson IBM Research Laboratory, Yorktown Heights, New York, United States of America
                [2 ]Department of Physiology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, United States of America
                Research Center Jülich, Germany
                Author notes

                The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AVA MB GAC. Performed the experiments: MB JAH MVC. Analyzed the data: LH MB GAC IR. Contributed reagents/materials/analysis tools: AVA GAC IR. Wrote the paper: AVA GAC.

                Article
                PCOMPBIOL-D-12-00350
                10.1371/journal.pcbi.1002719
                3486880
                23133342
                5cb02e50-36f3-43dc-baad-9ca928d7fbb8
                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
                : 1 March 2012
                : 15 August 2012
                Page count
                Pages: 12
                Funding
                This study was funded in part by NINDS NS35115 (AVA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Computational Biology
                Computational Neuroscience
                Neuroscience
                Cognitive Neuroscience
                Pain
                Neuroimaging
                Fmri

                Quantitative & Systems biology
                Quantitative & Systems biology

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