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Review
. 2007 Feb;53(2):271-86.
doi: 10.1016/j.brainresrev.2006.09.002. Epub 2006 Oct 6.

The neurocognitive bases of human multimodal food perception: consciousness

Affiliations
Review

The neurocognitive bases of human multimodal food perception: consciousness

Justus V Verhagen. Brain Res Rev. 2007 Feb.

Abstract

This review explores how we become aware of the (integrated) flavor of food. In recent years, progress has been made understanding the neural correlates of consciousness. Experimental and computational data have been largely based on the visual system. Contemporary neurobiological frameworks of consciousness are reviewed, concluding that neural reverberation among forward- and back-projecting neural ensembles across brain areas is a common theme. In an attempt to extrapolate these concepts to the oral-sensory and olfactory systems involved with multimodal flavor perception, the integration of the sensory information of which into a flavor gestalt has been reviewed elsewhere (Verhagen, J.V., Engelen, L., 2006. The neurocognitive bases of human multimodal food perception: Sensory integration. Neurosci. Biobehav. Rev. 30(5): 613_650), I reconceptualize the flavor-sensory system by integrating it into a larger neural system termed the Homeostatic Interoceptive System (HIS). This system consists of an oral (taste, oral touch, etc.) and non-oral part (non oral-thermosensation, pain, etc.) which are anatomically and functionally highly similar. Consistent with this new concept and with a large volume of experimental data, I propose that awareness of intraoral food is related to the concomitant reverberant self-sustained activation of a coalition of neuronal subsets in agranular insula and orbitofrontal cortex (affect, hedonics) and agranular insula and perirhinal cortex (food identity), as well as the amygdala (affect and identity) in humans. I further discuss the functional anatomy in relation essential nodes. These formulations are by necessity to some extent speculative.

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Figures

Fig. 1
Fig. 1
Schematic diagram of ascending neural pathways contributing to food perception. Several structures are omitted for simplicity. Brodmann's numerical labels indicated where known. Abbreviations (in order of appearance): LGN: lateral geniculate nucleus; V1, V2 and V4: visual areas 1, 2 and 4; TE/TEO: temporal(-occipital) visual areas; DCN: dorsal cochlear nucleus; SOC: superior olivary complex (non-obligatory relay); IC: inferior colliculus; MGN: medial geniculate nucleus; A1 and A2: auditory areas 1 and 2; mN5: motor nucleus of CN5; VPM(pc): (parvocellular part of the) ventroposteromedial nucleus of the thalamus; S1 and S2: somatosensory areas 1 and 2; spN5: spinal nucleus of CN5; NTS: nucleus of the solitary tract (r: rostral, c: caudal); G1, G2 and G3: gustatory areas 1, 2 and 3; Ig/FO: granular Insula/Frontal Operculum; Id: dysgranular Insula; Ia: agranular Insula; r/lIa: rostral/lateral Ia; OB: olfactory bulb; PC: piriform cortex; Ag: amygdala; OFC: orbitofrontal cortex; ACC: anterior cingulate cortex; PrC: perirhinal cortex; ErC: entorhinal cortex; HF: hippocampal formation. Based on (Norgren 1984; Barbas 1993; Baylis, Rolls et al. 1994; Heimer 1994; Cavada, Company et al. 2000; Mesulam 2000; Sewards and Sewards 2001; Craig 2002).
Fig. 2
Fig. 2
Top: The distribution of correlations between activity of single-units evoked by oral stimuli and behavioral acceptance ratings of these stimuli by macaque monkeys for three neural substrates. The distribution of OFC neurons, in contrast to that of neurons from AI/FO and Ag, appears bimodal, suggesting a stronger relation between hedonic evaluation of oral stimuli and the neural activity they evoke in OFC than in AI/FO and Ag (see text for details). Bottom: The distribution of the significance levels of these correlations was different between OFC on one hand and AI/FO and Ag on the other hand. Whereas only a small fraction of AI/FO and Ag neurons showed a significant (p<0.05) correlation between acceptability ratings and neural responses (12.1 and 11.4%, respectively), correlations of nearly half (39.6%) of the OFC neurons were significant.
Fig. 3
Fig. 3
To complement the individual neuronal-level analysis of Fig. 2, this figure provides a novel population-level analysis between the locations of stimuli on a 2-dimensional scale (MDS, a means to visualize neural population representation of stimuli; Systat v. 10, SPSS Inc.) and behavioral acceptability ratings (“Hedo”), and additionally between these locations and stimulus viscosity (“Visco”) and stimulus temperature (“Temp”). The five MDSs were based on stimulus response similarity as quantified by the Pearson correlation coefficient of the neural responses the stimuli evoked in each population. The figure shows for each area and monkey the r2 (the proportion of the variance explained) of the correlation (r) between stimulus location and these three factors as a function of the rotation of the MDS (no behavioral acceptiblity data was available for insula in monkey BK). Note that rotation of the MDS, as well as scaling, inversion and translation, yield equivalent MDS solutions. In all three neural areas of monkey BO viscosity correlated highly with MDS stimulus position (see Table 1 for details). Importantly, only at the level of the OFC did the behavioral acceptablity of stimuli (measured and analyzed separately for each monkey) correlate highly with the neural representation of the stimuli.
Fig. 4
Fig. 4
Proposed model of neural structures involved with the conscious experience of food. I propose that two different, but overlapping, large-scale networks are involved for 1) food object recognition awareness (Ia, PrC and Ag) and 2) food reward value awareness (Ia, OFC, ACC and Ag). Only the olfactory and gustatory (oHIS: oral division of the homeostatic interoceptive system) systems are shown for simplicity. Abbreviations: gr: gustatory receptors; NTS: nucleus of the solitary tract; VPMpc: parvocellular part of the ventroposteromedial nucleus of the thalamus; Ig/FO: granular Insula/Frontal Operculum; Id: dysgranular Insula; Ia: agranular Insula; PrC: perirhinal cortex; HF: hippocampal formation; Ag: amygdala; or: olfactory receptors; MOB: main olfactory bulb; PC: piriform cortex; EnP: endopyriform nucleus; OFC: orbitofrontal cortex; ACC: anterior cingulate cortex. Entorhinal cortex is incorporated in HF, and its direct connections with OB are not shown for clarity. Partially based on (Barbas 1993; Murray and Bussey 1999; Rolls 1999; Cavada, Company et al. 2000; Murray and Richmond 2001; Sewards and Sewards 2001).

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