Abstract
In a prior study, we showed that trying to detect a taste in a tasteless solution results in enhanced activity in the gustatory and attention networks. The aim of the current study was to use connectivity analyses to test if and how these networks interact during directed attention to taste. We predicted that the attention network modulates taste cortex, reflecting top-down enhancement of incoming sensory signals that are relevant to goal-directed behavior. fMRI was used to measure brain responses in 14 subjects as they performed two different tasks: (1) trying to detect a taste in a solution or (2) passively perceiving the same solution. We used psychophysiological interaction analysis to identify regions demonstrating increased connectivity during a taste attention task compared to passive tasting. We observed greater connectivity between the anterior cingulate cortex and the frontal eye fields, posterior parietal cortex, and parietal operculum and between the anterior cingulate cortex and the right anterior insula and frontal operculum. These results suggested that selective attention to taste is mediated by a hierarchical circuit in which signals are first sent from the frontal eye fields, posterior parietal cortex, and parietal operculum to the anterior cingulate cortex, which in turn modulates responses in the anterior insula and frontal operculum. We then tested this prediction using dynamic causal modeling. This analysis confirmed a model of indirect modulation of the gustatory cortex, with the strongest influence coming from the frontal eye fields via the anterior cingulate cortex. In summary, the results indicate that the attention network modulates the gustatory cortex during attention to taste and that the anterior cingulate cortex acts as an intermediary processing hub between the attention network and the gustatory cortex.
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References
Anderson JS, Ferguson MA et al (2010) Topographic maps of multisensory attention. Proc Natl Acad Sci 107(46):20110–20114
Bender G, Veldhuizen MG et al (2009) Neural correlates of evaluative compared with passive tasting. Eur J Neurosci 30(2):327–338
Boling W, Reutens DC et al (2002) Functional topography of the low postcentral area. J Neurosurg 97(2):388–395
Chun MM, Marois R (2002) The dark side of visual attention. Curr Opin Neurobiol 12(2):184–189
Corbetta M, Kincade MJ et al (2005) Neural basis and recovery of spatial attention deficits in spatial neglect. Nat Neurosci 8(11):1603–1610
Corbetta M, Patel G et al (2008) The reorienting system of the human brain: from environment to theory of mind. Neuron 58(3):306–324
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3(3):201–215
Craig AD (2009) How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70
Critchley HD, Wiens S et al (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7(2):189–195
De Araujo IE, Rolls ET et al (2003) Taste–olfactory convergence, and the representation of the pleasantness of flavour, in the human brain. Eur J Neurosci 18(7):2059–2068
Deen B, Pitskel NB et al (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21(7):1498–1506
Desseilles M, Schwartz S et al (2011) Depression alters "top-down" visual attention: a dynamic causal modeling comparison between depressed and healthy subjects. NeuroImage 54(2):1662–1668
Driver J, Frith C (2000) Shifting baselines in attention research. Nat Rev Neurosci 1(2):147–148
Friston KJ, Buechel C et al (1997) Psychophysiological and modulatory interactions in neuroimaging. NeuroImage 6(3):218–229
Friston KJ, Harrison L et al (2003) Dynamic causal modelling. NeuroImage 19(4):1273–1302
Friston KJ, Holmes AP et al (1995) Statistical parametric maps in functional imaging. Human brain mapp 2:189–210
Gitelman DR, Penny WD et al (2003) Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. NeuroImage 19(1):200–207
Grabenhorst F, Rolls ET (2010) Attentional modulation of affective versus sensory processing: functional connectivity and a top-down biased activation theory of selective attention. J Neurophysiol 104(3):1649–1660
Green BG (2003) Studying taste as a cutaneous sense. Food Quality Pref 14(2):99–109
Grefkes C, Wang LE et al (2010) Noradrenergic modulation of cortical networks engaged in visuomotor processing. Cereb Cortex 20(4):783–797
Henson RN, Price CJ et al (2002) Detecting latency differences in event-related BOLD responses: application to words versus nonwords and initial versus repeated face presentations. NeuroImage 15(1):83–97
Hopfinger JB, Buonocore MH et al (2000) The neural mechanisms of top-down attentional control. Nat Neurosci 3(3):284–291
Kanwisher N, Wojciulik E (2000) Visual attention: insights from brain imaging. Nat Rev Neurosci 1(2):91–100
Kastner S, Pinsk MA et al (1999) Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron 22(4):751–761
Kincade JM, Abrams RA et al (2005) An event-related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. J Neurosci 25(18):4593–4604
Kobayakawa T, Endo H et al (1996) The primary gustatory area in human cerebral cortex studied by magnetoencephalography. Neurosci Lett 212(3):155–158
Kobayakawa T, Ogawa H et al (1999) Spatio-temporal analysis of cortical activity evoked by gustatory stimulation in humans. Chem Senses 24(2):201–209
Kurth F, Zilles K et al (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214(5):519–534
Luck SJ, Chelazzi L et al (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol 77(1):24–42
Marciani L, Pfeiffer JC et al (2006) Improved methods for fMRI studies of combined taste and aroma stimuli. J Neurosci Methods 158(2):186–194
Marks LE (2002) The role of attention in chemosensation. Food Quality Pref 14:147–155
Marks LE, Wheeler ME (1998) Attention and the detectability of weak taste stimuli. Chem Senses 23(1):19–29
Menon V, Uddin L (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214(5):655–667
Mesulam M, Small DM et al (2005) A heteromodal large-scale network for spatial attention. In: Itti L, Rees G, Tsotsos J (eds) Neurobiology of attention. Elsevier, San Diego, pp 29–34
Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. III: efferent cortical output and comments on function. J Comp Neurol 212(1):38–52
Mesulam MM, Mufson EJ (1985) The insula of Reil in man and monkey. Cereb Cortex 4:179–225
O'Doherty J, Rolls ET et al (2001) Representation of pleasant and aversive taste in the human brain. J Neurophysiol 85(3):1315–1321
Ogawa H, Wakita M et al (2005) Functional MRI detection of activation in the primary gustatory cortices in humans. Chem Senses 30(7):583–592
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9(1):97–113
Penfield W, Boldrey E (1937) Somatic and motor sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 60:389–443
Penny WD, Stephan KE et al (2010) Comparing families of dynamic causal models. PLoS Comput Biol 6(3):e1000709
Pessoa L, Kastner S et al (2003) Neuroimaging studies of attention: from modulation of sensory processing to top-down control. J Neurosci 23(10):3990–3998
Posner MI (1980) Orienting of attention. Q J Exp Psychol 32(1):3–25
Posner MI, Sheese BE et al (2006) Analyzing and shaping human attentional networks. Neural Networks 19(9):1422–1429
Posner MI, Snyder CR et al (1980) Attention and the detection of signals. J Exp Psychol 109(2):160–174
Pritchard TC, Hamilton RB et al (1986) Projections of thalamic gustatory and lingual areas in the monkey, Macaca fascicularis. J Comp Neurol 244(2):213–228
Pugh KR, Shaywitz BA et al (1996) Auditory selective attention: an fMRI investigation. NeuroImage 4(3 Pt 1):159–173
Shulman GL, Ollinger JM et al (1999) Areas involved in encoding and applying directional expectations to moving objects. J Neurosci 19(21):9480–9496
Small DM (2008) Flavor and the formation of category specific processing in olfaction. Chemosens Percept 1:136–146
Small DM, Gerber JC et al (2005) Differential neural responses evoked by orthonasal versus retronasal odorant perception in humans. Neuron 47(4):593–605
Small DM, Gregory MD et al (2003) Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron 39(4):701–711
Small DM, Voss J et al (2004) Experience-dependent neural integration of taste and smell in the human brain. J Neurophysiol 92(3):1892–1903
Smith SM, Miller KL et al (2011) Network modelling methods for FMRI. NeuroImage 54(2):875–891
Stephan KE, Penny WD et al (2009) Bayesian model selection for group studies. NeuroImage 46(4):1004–1017
Stephan KE, Penny WD et al (2010) Ten simple rules for dynamic causal modeling. NeuroImage 49(4):3099–3109
Talairach J, Tournoux P (1998) Co-planar stereotaxic atlas of the human brain. Thieme, New York
Todrank J, Bartoshuk LM (1991) A taste illusion: taste sensation localized by touch. Physiol Behav 50(5):1027–1031
Uddin LQ, Supekar K et al (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20(11):2636–2646
van den Heuvel MP, Mandl RCW et al (2009) Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Human Brain Mapp 30(10):3127–3141
Veldhuizen MG, Bender G et al (2007) Trying to detect taste in a tasteless solution: modulation of early gustatory cortex by attention to taste. Chem Senses 32(6):569–581
Veldhuizen MG, Douglas D et al (2011) The anterior insular cortex represents breaches of taste identity expectation. J Neurosci 31(41):14735–14744
Veldhuizen MG, Small DM (2011) Modality-specific neural effects of selective attention to taste and odor. Chem Senses 36(8):747–760
Voisin J, Bidet-Caulet A et al (2006) Listening in silence activates auditory areas: a functional magnetic resonance imaging study. J Neurosci 26(1):273–278
Worsley KJ, Friston KJ (1995) Analysis of fMRI time-series revisited—again. NeuroImage 2(3):173–181
Zald DH, Lee JT et al (1998) Aversive gustatory stimulation activates limbic circuits in humans. Brain 121(Pt 6):1143–1154
Zelano C, Bensafi M et al (2005) Attentional modulation in human primary olfactory cortex. Nat Neurosci 8(1):114–120
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This study was supported by NIDCD R016706-01 awarded to DMS.
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Veldhuizen, M.G., Gitelman, D.R. & Small, D.M. An fMRI Study of the Interactions Between the Attention and the Gustatory Networks. Chem. Percept. 5, 117–127 (2012). https://doi.org/10.1007/s12078-012-9122-z
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DOI: https://doi.org/10.1007/s12078-012-9122-z