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      The Neuronal Encoding of Oral Fat by the Coefficient of Sliding Friction in the Cerebral Cortex and Amygdala

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          Abstract

          Fat in the diet contributes to the pleasant mouthfeel of many foods, but overconsumption may contribute to obesity. Here we analyze what properties of fat in the mouth are sensed, by analyzing the responses of neurons in the macaque insular taste cortex, and two areas to which it projects the orbitofrontal cortex where the pleasantness of fat is represented, and the amygdala. We discovered that the firing rate responses of these fat-responsive neurons are correlated with the coefficient of sliding friction (CSF) and not with viscosity which reflects food thickness. Other, not fat-sensitive, neurons encoded viscosity and not the CSF. Neuronal population analyses confirmed that fat-responsive neurons conveyed information about the CSF but not about viscosity. Conversely the viscosity-sensitive neuronal population conveyed information about viscosity but not about the CSF. This new understanding of the representation of oral fat in the cerebral cortex and amygdala opens the way for the systematic development of foods with the pleasant mouthfeel of fat, together with ideal nutritional content and has great potential to contribute to healthy eating and a healthy body weight.

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          Most cited references38

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          Taste, olfactory, and food reward value processing in the brain.

          Complementary neuronal recordings in primates, and functional neuroimaging in humans, show that the primary taste cortex in the anterior insula provides separate and combined representations of the taste, temperature, and texture (including fat texture) of food in the mouth independently of hunger and thus of reward value and pleasantness. One synapse on, in a second tier of processing, in the orbitofrontal cortex, these sensory inputs are for some neurons combined by associative learning with olfactory and visual inputs, and these neurons encode food reward value on a continuous scale in that they only respond to food when hungry, and in that activations correlate linearly with subjective pleasantness. Cognitive factors, including word-level descriptions, and selective attention to affective value, modulate the representation of the reward value of taste and olfactory stimuli in the orbitofrontal cortex and a region to which it projects, the anterior cingulate cortex, a tertiary taste cortical area. The food reward representations formed in this way play an important role in the control of appetite, and food intake. Individual differences in these reward representations may contribute to obesity, and there are age-related differences in these value representations that shape the foods that people in different age groups find palatable. In a third tier of processing in medial prefrontal cortex area 10, decisions between stimuli of different reward value are taken, by attractor decision-making networks.
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            Hunger and satiety modify the responses of olfactory and visual neurons in the primate orbitofrontal cortex.

            1. The primate orbitofrontal cortex is the site of convergence of information from primary taste and primary olfactory cortical regions. In addition, it receives projections from temporal lobe visual areas concerned with the representation of objects such as foods. Previous work has shown that the responses of gustatory neurons in the secondary taste area within the orbitofrontal cortex are modulated by hunger and satiety, in that they stop responding to the taste of a food on which an animal has been fed to behavioral satiation, yet may continue to respond to the taste of other foods. 2. This study demonstrates a similar modulation of the responses of olfactory and visual orbitofrontal cortex neurons after feeding to satiety. Seven of nine olfactory neurons that were responsive to the odors of foods, such as blackcurrant juice, were found to decrease their responses to the odor of the satiating food in a selective and statistically significant manner. 3. It also was found for eight of nine neurons that had selective responses to the sight of food, that they demonstrated a sensory-specific reduction in their visual responses to foods after satiation. 4. The responses of orbitofrontal cortex neurons selective for foods in more than one modality also were analyzed before and after feeding to satiation. Satiety often affected the responses of these multimodal neurons across all modalities, but a sensory-specific effect was not always demonstrable for both modalities. 5. These findings show that the olfactory and visual representations of food, as well as the taste representation of food, in the primate orbitofrontal cortex are modulated by hunger. Usually a component related to sensory-specific satiety can be demonstrated. The findings link at least part of the processing of olfactory and visual information in this brain region to the control of feeding-related behavior.
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              The neuronal encoding of information in the brain.

              We describe the results of quantitative information theoretic analyses of neural encoding, particularly in the primate visual, olfactory, taste, hippocampal, and orbitofrontal cortex. Most of the information turns out to be encoded by the firing rates of the neurons, that is by the number of spikes in a short time window. This has been shown to be a robust code, for the firing rate representations of different neurons are close to independent for small populations of neurons. Moreover, the information can be read fast from such encoding, in as little as 20 ms. In quantitative information theoretic studies, only a little additional information is available in temporal encoding involving stimulus-dependent synchronization of different neurons, or the timing of spikes within the spike train of a single neuron. Feature binding appears to be solved by feature combination neurons rather than by temporal synchrony. The code is sparse distributed, with the spike firing rate distributions close to exponential or gamma. A feature of the code is that it can be read by neurons that take a synaptically weighted sum of their inputs. This dot product decoding is biologically plausible. Understanding the neural code is fundamental to understanding not only how the cortex represents, but also processes, information. Copyright © 2011 Elsevier Ltd. All rights reserved.
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                Author and article information

                Journal
                Cereb Cortex
                Cereb. Cortex
                cercor
                Cerebral Cortex (New York, NY)
                Oxford University Press
                1047-3211
                1460-2199
                November 2018
                31 August 2018
                31 August 2018
                : 28
                : 11
                : 4080-4089
                Affiliations
                [1 ]Oxford Centre for Computational Neuroscience, Oxford, England; and University of Warwick, Department of Computer Science, Coventry, England
                [2 ]School of Chemical Engineering, University of Birmingham, Birmingham, England
                Author notes
                Address Correspondence to Professor Edmund T. Rolls, Email: Edmund.Rolls@ 123456oxcns.org
                Author information
                http://orcid.org/0000-0003-3025-1292
                Article
                bhy213
                10.1093/cercor/bhy213
                6188542
                30169795
                d72d8b26-77f7-488f-9666-88499a7c5b75
                © The Author(s) 2018. Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@ 123456oup.com

                History
                : 15 June 2018
                : 05 August 2018
                : 07 August 2018
                Page count
                Pages: 10
                Funding
                Funded by: Engineering and Physical Sciences Research Council 10.13039/501100000266
                Award ID: EP/K030957/1
                Categories
                Original Articles

                Neurology
                fat texture,food texture,insula,nutrition,orbitofrontal cortex
                Neurology
                fat texture, food texture, insula, nutrition, orbitofrontal cortex

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