Gustatory processing: a dynamic systems approach

Recent gustatory studies have provided a growing body of evidence that taste processing is dynamic and distributed, and the taste system too complex to be adequately described by traditional feed-forward models of taste coding. Current research demonstrates that neuronal responses throughout the gustatory neuroaxis are broad, variable and temporally structured, as a result of the fact that the taste network is extensive and heavily interconnected, containing modulatory pathways, many of which are reciprocal. Multimodal influences (e.g. olfactory and somatosensory) and effects of internal state (e.g. attention and expectation), shown in both behavioral and neuronal responses to taste stimuli, add further complexity to neural taste responses. Future gustatory research should extend to more brain regions, incorporate more connections, and analyze behaviors and neuronal responses in both time- and state-dependent manners.

[1]  Y. Dudai,et al.  The Role of Identified Neurotransmitter Systems in the Response of Insular Cortex to Unfamiliar Taste: Activation of ERK1–2 and Formation of a Memory Trace , 2000, The Journal of Neuroscience.

[2]  B. Halpern,et al.  Taste Stimuli: Quality Coding Time , 1971, Science.

[3]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[4]  David V. Smith,et al.  Neuronal cell types and taste quality coding , 2000, Physiology & Behavior.

[5]  Mriganka Sur,et al.  Local networks in visual cortex and their influence on neuronal responses and dynamics , 2004, Journal of Physiology-Paris.

[6]  M. Packard,et al.  Amygdala and “emotional” modulation of the relative use of multiple memory systems , 2004, Neurobiology of Learning and Memory.

[7]  A. Faurion,et al.  Modulation of taste peripheral signal through interpapillar inhibition in hamsters , 2004, Neuroscience Letters.

[8]  F. Toates,et al.  Feeding and drinking , 1987 .

[9]  N. Onoda,et al.  Convergence of olfactory and gustatory connections onto the endopiriform nucleus in the rat , 2004, Neuroscience.

[10]  J. Alonso,et al.  Thalamic Burst Mode and Inattention in the Awake LGNd , 2006, Neuron.

[11]  David V. Smith,et al.  Medullary taste responses are modulated by the bed nucleus of the stria terminalis. , 2005, Chemical senses.

[12]  J. Bureš,et al.  [Conditioned taste aversion]. , 1977, Ceskoslovenska fysiologie.

[13]  Jeffrey M. Zacks,et al.  Coherent spontaneous activity accounts for trial-to-trial variability in human evoked brain responses , 2006, Nature Neuroscience.

[14]  S. Reilly,et al.  Conditioned taste aversion and amygdala lesions in the rat: A critical review , 2005, Neuroscience & Biobehavioral Reviews.

[15]  N. Ryba,et al.  The Receptors for Mammalian Sweet and Umami Taste , 2003, Cell.

[16]  Sidney A. Simon,et al.  Neural Ensemble Coding of Satiety States , 2006, Neuron.

[17]  G. Laurent,et al.  Transient Dynamics versus Fixed Points in Odor Representations by Locust Antennal Lobe Projection Neurons , 2005, Neuron.

[18]  Yehezkel Yeshurun,et al.  Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation , 2006, NeuroImage.

[19]  Edward E. Smith,et al.  Altering expectancy dampens neural response to aversive taste in primary taste cortex , 2006, Nature Neuroscience.

[20]  L. Jarrard,et al.  A role for hippocampus in the utilization of hunger signals. , 1993, Behavioral and neural biology.

[21]  T Kobayakawa,et al.  Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. , 1999, Chemical senses.

[22]  J. Travers,et al.  Motor and Premotor Mechanisms of Licking , 1997, Neuroscience & Biobehavioral Reviews.

[23]  H. S. Garven,et al.  Ganglion cells in the mammalian tongue. , 1952, Journal of Physiology.

[24]  Alfredo Fontanini,et al.  7 to 12 Hz activity in rat gustatory cortex reflects disengagement from a fluid self-administration task. , 2005, Journal of neurophysiology.

[25]  H. Grill,et al.  Intraoral intake and taste reactivity responses elicited by sucrose and sodium chloride in chronic decerebrate rats. , 1988, Behavioral neuroscience.

[26]  T. Sejnowski,et al.  Fast Odor Learning Improves Reliability of Odor Responses in the Locust Antennal Lobe , 2005, Neuron.

[27]  D. Weinberger,et al.  Ibotenic acid lesion of the ventral hippocampus differentially affects dopamine and its metabolites in the nucleus accumbens and prefrontal cortex in the rat , 1992, Brain Research.

[28]  L. Jarrard,et al.  The hippocampus and motivation revisited: appetite and activity , 2001, Behavioural Brain Research.

[29]  R. Zatorre,et al.  Odor-induced changes in taste perception , 2004, Experimental Brain Research.

[30]  L. Marks,et al.  Effect of endogenous attention on detection of weak gustatory and olfactory flavors , 2004, Perception & psychophysics.

[31]  E. Delay,et al.  Sucrose and monosodium glutamate taste thresholds and discrimination ability of T1R3 knockout mice. , 2006, Chemical senses.

[32]  D. Hill Neural plasticity in the gustatory system. , 2004, Nutrition reviews.

[33]  E. Ahissar,et al.  Neural signature of taste familiarity in the gustatory cortex of the freely behaving rat. , 2004, Journal of neurophysiology.

[34]  Takashi Yamamoto,et al.  Conditioned taste aversion in rats with excitotoxic brain lesions , 1995, Neuroscience Research.

[35]  M. Nicolelis,et al.  Dynamic and Multimodal Responses of Gustatory Cortical Neurons in Awake Rats , 2001, The Journal of Neuroscience.

[36]  A. Ghazanfar,et al.  Is neocortex essentially multisensory? , 2006, Trends in Cognitive Sciences.

[37]  M. Nicolelis,et al.  Gustatory processing is dynamic and distributed , 2002, Current Opinion in Neurobiology.

[38]  Z. Karádi,et al.  Centrifugal inputs modulate taste aversion learning associated parabrachial neuronal activities. , 2004, Journal of neurophysiology.

[39]  Michael L. Lavine,et al.  Rapid Taste Responses in the Gustatory Cortex during Licking , 2006, The Journal of Neuroscience.

[40]  N. Ryba,et al.  The receptors and coding logic for bitter taste , 2005, Nature.

[41]  松尾 龍二 Conditioned Taste Aversion-Memory of a Special Kind : Oxford Psychology Series, Jan Bures, Federico Bermudez-Rattoni, 山本隆著, 192頁, 18,150円, Oxford University Press, 1998年, ISBN 019 8523475 , 1999 .

[42]  H. Eichenbaum Hippocampus Cognitive Processes and Neural Representations that Underlie Declarative Memory , 2004, Neuron.

[43]  Makoto Honjo,et al.  To-and-fro optical voltage signal propagation between the insular gustatory and parietal oral somatosensory areas in rat cortex slices , 2004, Brain Research.

[44]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[45]  J. Victor,et al.  Taste response variability and temporal coding in the nucleus of the solitary tract of the rat. , 2003, Journal of neurophysiology.

[46]  R. Norgren,et al.  Activity in the hypothalamus, amygdala, and cortex generates bilateral and convergent modulation of pontine gustatory neurons. , 2004, Journal of neurophysiology.

[47]  D. Mumford,et al.  Neural activity in early visual cortex reflects behavioral experience and higher-order perceptual saliency , 2002, Nature Neuroscience.

[48]  Kristin Scott,et al.  Imaging Taste Responses in the Fly Brain Reveals a Functional Map of Taste Category and Behavior , 2006, Neuron.

[49]  David V. Smith,et al.  Neural representation of bitter taste in the nucleus of the solitary tract. , 2005, Journal of neurophysiology.

[50]  H. Grill,et al.  Central gustatory lesions: II. Effects on sodium appetite, taste aversion learning, and feeding behaviors. , 1991, Behavioral neuroscience.

[51]  Goran Hellekant,et al.  Sense of taste in a New World monkey, the common marmoset. II. Link between behavior and nerve activity. , 2004, Journal of neurophysiology.

[52]  Miguel A L Nicolelis,et al.  Orbitofrontal ensemble activity monitors licking and distinguishes among natural rewards. , 2006, Journal of neurophysiology.

[53]  David V. Smith,et al.  Influence of Response Variability on the Coding Performance of Central Gustatory Neurons , 2006, The Journal of Neuroscience.

[54]  Toshihide Sato,et al.  Taste cell responses in the frog are modulated by parasympathetic efferent nerve fibers. , 2005, Chemical senses.

[55]  David A. Bulkin,et al.  Seeing sounds: visual and auditory interactions in the brain , 2006, Current Opinion in Neurobiology.

[56]  Noriaki Hattori,et al.  Functional Imaging of Gustatory Perception and Imagery: Btop-downq Processing of Gustatory Signals , 2004 .

[57]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[58]  M. Weliky,et al.  Small modulation of ongoing cortical dynamics by sensory input during natural vision , 2004, Nature.

[59]  Miguel A L Nicolelis,et al.  Taste-Specific Neuronal Ensembles in the Gustatory Cortex of Awake Rats , 2002, The Journal of Neuroscience.

[60]  Functional reciprocal connections between olfactory and gustatory pathways. , 2005, Chemical senses.

[61]  D. Katz,et al.  Hippocampal inactivation enhances taste learning. , 2005, Learning & memory.

[62]  David V. Smith,et al.  Modulation of parabrachial taste neurons by electrical and chemical stimulation of the lateral hypothalamus and amygdala. , 2005, Journal of neurophysiology.

[63]  Y. Dudai,et al.  Memory Extinction, Learning Anew, and Learning the New: Dissociations in the Molecular Machinery of Learning in Cortex , 2001, Science.

[64]  D. Small,et al.  Odor/taste integration and the perception of flavor , 2005, Experimental Brain Research.