Affective value, intensity and quality of liquid tastants/food discernment in the human brain: An activation likelihood estimation meta-analysis

ABSTRACT The primary dimensions of taste are affective value, intensity and quality. Numerous studies have reported the role of the insula in evaluating these dimensions of taste; however, the results were inconsistent. Therefore, in the current study, we performed meta‐analyses of published data to identify locations consistently activated across studies and evaluate whether different regions of the human brain could be responsible for processing different dimensions of taste. Meta‐analyses were performed on 39 experiments, with 846 total healthy subjects (without psychiatric/neurological disorders) in 34 studies reporting whole‐brain results. The aim was to establish the activation likelihood estimation (ALE) of taste‐mediated regional activation across the whole brain. Apart from one meta‐analysis for all studies in general, three analyses were performed to reveal the clusters of activation that were attributable to processing the affective value (data from 323 foci), intensity (data from 43 foci) and quality (data from 45 foci) of taste. The ALE revealed eight clusters of activation outside the insula for processing affective value, covering the middle and posterior cingulate, pre‐/post‐central gyrus, caudate and thalamus. The affective value had four clusters of activation (two in each hemisphere) in the insula. The intensity and quality activated only the insula, each with one cluster on the right. The concurrence between studies was moderate; at best, 53% of the experiments contributed to the significant clusters attributable to the affective value, 60% to intensity and 50% to quality. The affective value was processed bilaterally in the anterior to middle insula, whereas intensity was processed in the right antero‐middle insula, and quality was processed in the right middle insula. The right middle dorsal insula was responsible for processing both the affective value and quality of taste. The exploratory analysis on taste quality did not have a significant result if the studies using liquid food stimuli were excluded. Results from the meta‐analyses on studies involving the oral delivery of liquid tastants or liquid food stimuli confirmed that the insula is involved in processing all three dimensions of taste. More experimental studies are required to investigate whether brain activations differ between liquid tastants and food. The coordinates of activated brain areas and brain maps are provided to serve as references for future taste/food studies. HighlightsData was pooled from 34 whole‐brain taste fMRI papers (39 experiments, 846 subjects).Affective value of taste appeared to be processed by bilateral anterior and middle insula, cingulate cortex, striatum and orbitofrontal cortexIntensity of taste was processed in right antero‐middle insula.Quality of taste was processed in right middle dorsal insula.This study provided brain maps and coordinates for future taste/food studies.

[1]  Toshiko Tanaka,et al.  Diverse tastes: Genetics of sweet and bitter perception , 2006, Physiology & Behavior.

[2]  P. Cowen,et al.  The D2 antagonist sulpiride modulates the neural processing of both rewarding and aversive stimuli in healthy volunteers , 2011, Psychopharmacology.

[3]  Lionel Pazart,et al.  An fMRI study on the influence of sommeliers' expertise on the integration of flavor , 2014, Front. Behav. Neurosci..

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

[5]  P. Cowen,et al.  Effects of pramipexole on the processing of rewarding and aversive taste stimuli , 2013, Psychopharmacology.

[6]  Max A. Viergever,et al.  What you see is what you eat: An ALE meta-analysis of the neural correlates of food viewing in children and adolescents , 2015, NeuroImage.

[7]  J. Fudge,et al.  Altered insula response to sweet taste processing after recovery from anorexia and bulimia nervosa. , 2013, The American journal of psychiatry.

[8]  T. R. Scott,et al.  Taste in the Monkey Cortex , 1999, Physiology & Behavior.

[9]  V. Rocha-Rego,et al.  Investigating the Predictive Value of Functional MRI to Appetitive and Aversive Stimuli: A Pattern Classification Approach , 2016, PloS one.

[10]  Johan N Lundström,et al.  Identification of human gustatory cortex by activation likelihood estimation , 2011, Human brain mapping.

[11]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[12]  Andy Wai Kan Yeung,et al.  Basic taste processing recruits bilateral anteroventral and middle dorsal insulae: An activation likelihood estimation meta‐analysis of fMRI studies , 2017, Brain and behavior.

[13]  Fabian Grabenhorst,et al.  How cognition modulates affective responses to taste and flavor: top-down influences on the orbitofrontal and pregenual cingulate cortices. , 2008, Cerebral cortex.

[14]  K. Zilles,et al.  A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis , 2010, Brain Structure and Function.

[15]  R J Zatorre,et al.  Human cortical gustatory areas: a review of functional neuroimaging data. , 1999, Neuroreport.

[16]  Remco J. Renken,et al.  Functional specialization of the male insula during taste perception , 2015, NeuroImage.

[17]  Thomas Hummel,et al.  Oral texture influences the neural processing of ortho- and retronasal odors in humans , 2014, Brain Research.

[18]  G. Buracas,et al.  On-line psychophysical data acquisition and event-related fMRI protocol optimized for the investigation of brain activation in response to gustatory stimuli , 2007, Journal of Neuroscience Methods.

[19]  Jed A. Meltzer,et al.  Neural correlates of evaluative compared with passive tasting , 2009, The European journal of neuroscience.

[20]  T. Yoshiura,et al.  Localization of brain activation by umami taste in humans , 2011, Brain Research.

[21]  Simon B Eickhoff,et al.  Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses , 2012, Human brain mapping.

[22]  M. Mesulam,et al.  Dissociation of Neural Representation of Intensity and Affective Valuation in Human Gustation , 2003, Neuron.

[23]  Catherine J. Harmer,et al.  Opposing neural effects of naltrexone on food reward and aversion: implications for the treatment of obesity , 2014, Psychopharmacology.

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

[25]  Fabian Grabenhorst,et al.  Selective attention to affective value alters how the brain processes taste stimuli , 2008, The European journal of neuroscience.

[26]  High resolution time–intensity recording with synchronized solution delivery system for the human dynamic taste perception , 2015, Journal of Neuroscience Methods.

[27]  J. Hudry,et al.  Dietary fat induces sustained reward response in the human brain without primary taste cortex discrimination , 2013, Front. Hum. Neurosci..

[28]  G. Paxinos,et al.  Atlas of the Human Brain Ed. 4 , 2016 .

[29]  P. Cowen,et al.  Neural Effects of Cannabinoid CB1 Neutral Antagonist Tetrahydrocannabivarin on Food Reward and Aversion in Healthy Volunteers , 2015, The international journal of neuropsychopharmacology.

[30]  V. Gallese,et al.  Emotional susceptibility trait modulates insula responses and functional connectivity in flavor processing , 2015, Front. Behav. Neurosci..

[31]  Angela R. Laird,et al.  Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation , 2016, NeuroImage.

[32]  Dana M Small,et al.  Modality-specific neural effects of selective attention to taste and odor. , 2011, Chemical senses.

[33]  D. Briggs,et al.  An Evolutionary Perspective , 2004, J. Decis. Syst..

[34]  Erin Green,et al.  Age-related functional changes in gustatory and reward processing regions: An fMRI study , 2010, NeuroImage.

[35]  S. Sheen,et al.  Testing a tool for assessing the risk of bias for nonrandomized studies showed moderate reliability and promising validity. , 2013, Journal of clinical epidemiology.

[36]  E. Rolls,et al.  Taste‐olfactory convergence, and the representation of the pleasantness of flavour, in the human brain , 2003, The European journal of neuroscience.

[37]  P. Smeets,et al.  You are what you eat : A neuroscience perspective on consumers' personality characteristics as determinants of eating behavior , 2015 .

[38]  P. Cowen,et al.  Neural Processing of Reward and Punishment in Young People at Increased Familial Risk of Depression , 2012, Biological Psychiatry.

[39]  Angela R. Laird,et al.  Activation likelihood estimation meta-analysis revisited , 2012, NeuroImage.

[40]  K. Sawyer The Cognitive Neuroscience of Creativity: A Critical Review , 2011 .

[41]  L. Epstein,et al.  Multilocus Genetic Composite Reflecting Dopamine Signaling Capacity Predicts Reward Circuitry Responsivity , 2012, The Journal of Neuroscience.

[42]  B. Popkin,et al.  Trends of obesity and underweight in older children and adolescents in the United States, Brazil, China, and Russia. , 2002, The American journal of clinical nutrition.

[43]  Edmund T Rolls,et al.  Enhanced affective brain representations of chocolate in cravers vs. non‐cravers , 2007, The European journal of neuroscience.

[44]  D. Small,et al.  Evidence for an integrated oral sensory module in the human anterior ventral insula. , 2010, Chemical senses.

[45]  Andy Wai Kan Yeung,et al.  Enhancement of Combined Umami and Salty Taste by Glutathione in the Human Tongue and Brain. , 2016, Chemical senses.

[46]  Ulrike Toepel,et al.  Visual-Gustatory Interaction: Orbitofrontal and Insular Cortices Mediate the Effect of High-Calorie Visual Food Cues on Taste Pleasantness , 2012, PloS one.

[47]  Lori Haase,et al.  Cortical activation in response to pure taste stimuli during the physiological states of hunger and satiety , 2009, NeuroImage.

[48]  Lori Haase,et al.  Males and females show differential brain activation to taste when hungry and sated in gustatory and reward areas , 2011, Appetite.

[49]  Andy Wai Kan Yeung,et al.  Taste intensity modulates effective connectivity from the insular cortex to the thalamus in humans , 2016, NeuroImage.

[50]  Matthew A. Lambon Ralph,et al.  The variation of function across the human insula mirrors its patterns of structural connectivity: Evidence from in vivo probabilistic tractography , 2012, NeuroImage.

[51]  P. Arabie,et al.  TASTE INTENSITY AS A FUNCTION OF STIMULUS CONCENTRATION AND SOLVENT VISCOSITY. , 1970, Journal of texture studies.

[52]  E. Stice,et al.  Relative ability of fat and sugar tastes to activate reward, gustatory, and somatosensory regions. , 2013, The American journal of clinical nutrition.

[53]  E. Stice,et al.  Neural responsivity during soft drink intake, anticipation, and advertisement exposure in habitually consuming youth , 2014, Obesity.

[54]  Max A. Viergever,et al.  The first taste is always with the eyes: A meta-analysis on the neural correlates of processing visual food cues , 2011, NeuroImage.

[55]  P. Breslin,et al.  An Evolutionary Perspective on Food and Human Taste , 2013, Current Biology.

[56]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[57]  K. Zilles,et al.  Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: A random‐effects approach based on empirical estimates of spatial uncertainty , 2009, Human brain mapping.

[58]  T. Yoshiura,et al.  Localization of the primary taste cortex by contrasting passive and attentive conditions , 2013, Experimental Brain Research.

[59]  Edmund T Rolls,et al.  Representation in the Human Brain of Food Texture and Oral Fat , 2004, The Journal of Neuroscience.

[60]  J. Hudry,et al.  Electrical neuroimaging reveals intensity-dependent activation of human cortical gustatory and somatosensory areas by electric taste , 2010, Biological Psychology.

[61]  Hiroshi Honda,et al.  The temporal change in the cortical activations due to salty and sweet tastes in humans: fMRI and time–intensity sensory evaluation , 2012, Neuroreport.

[62]  Dana M. Small,et al.  Taste representation in the human insula , 2010, Brain Structure and Function.

[63]  M A Viergever,et al.  Representation of sweet and salty taste intensity in the brain. , 2010, Chemical senses.

[64]  L. Haase,et al.  Can age-related CNS taste differences be detected as early as middle age? Evidence from fMRI , 2013, Neuroscience.

[65]  L. Marciani,et al.  Use of an Immediate Swallow Protocol to Assess Taste and Aroma Integration in fMRI Studies , 2011 .

[66]  Ellen Poliakoff,et al.  Expected taste intensity affects response to sweet drinks in primary taste cortex , 2011, Neuroreport.

[67]  J. Mattingley,et al.  Understanding the minds of others: A neuroimaging meta-analysis , 2016, Neuroscience & Biobehavioral Reviews.

[68]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[69]  Sébastien M. Crouzet,et al.  Taste Quality Decoding Parallels Taste Sensations , 2015, Current Biology.

[70]  N. Ryba,et al.  The receptors and cells for mammalian taste , 2006, Nature.

[71]  Guinevere F. Eden,et al.  Meta-Analysis of the Functional Neuroanatomy of Single-Word Reading: Method and Validation , 2002, NeuroImage.

[72]  R B Hamilton,et al.  Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis , 1986, The Journal of comparative neurology.

[73]  Angela R Laird,et al.  Neural Bases Of Food Perception: Coordinate-Based Meta-Analyses Of Neuroimaging Studies In Multiple Modalities , 2013, Obesity.

[74]  J. Verhagen,et al.  The neurocognitive bases of human multimodal food perception: Sensory integration , 2006, Neuroscience & Biobehavioral Reviews.

[75]  M M Mesulam,et al.  Thalamic connections of the insula in the rhesus monkey and comments on the paralimbic connectivity of the medial pulvinar nucleus , 1984, The Journal of comparative neurology.

[76]  R Todd Constable,et al.  Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste. , 2007, Chemical senses.

[77]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[78]  Rose Marie Pangborn,et al.  Individual variation in affective responses to taste stimuli , 1970 .

[79]  N. Sadato,et al.  The Brain Mechanisms Underlying the Perception of Pungent Taste of Capsaicin and the Subsequent Autonomic Responses , 2016, Front. Hum. Neurosci..