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Identification of Human Gustatory Cortex by Activation Likelihood Estimation

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Identification of Human Gustatory Cortex by Activation Likelihood Estimation r Human Brain Mapping 32:2256–2266 (2011) r Identification of Human Gustatory Cortex by Activation Likelihood Estimation Maria G. Veldhuizen,1,2 Jessica Albrecht,3 Christina Zelano,4 Sanne Boesveldt,3 Paul Breslin,3,5 and Johan N. Lundstro¨m3,6,7* 1Affective Sensory Neuroscience, John B. Pierce Laboratory, New Haven, Connecticut 2Department of Psychiatry, Yale University School of Medicine, New Haven, Connecticut 3Monell Chemical Senses Center, Philadelphia, Pennsylvania 4Department of Neurology, Northwestern University, Chicago, Illinois 5Department of Nutritional Sciences, Rutgers University School of Environmental and Biological Sciences, New Brunswick, New Jersey 6Department of Psychology, University of Pennsylvania, Philadelphia, Pennsylvania 7Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden r r Abstract: Over the last two decades, neuroimaging methods have identified a variety of taste-responsive brain regions. Their precise location, however, remains in dispute. For example, taste stimulation activates areas throughout the insula and overlying operculum, but identification of subregions has been inconsistent. Furthermore, literature reviews and summaries of gustatory brain activations tend to reiterate rather than resolve this ambiguity. Here, we used a new meta-analytic method [activation likelihood estimation (ALE)] to obtain a probability map of the location of gustatory brain activation across 15 studies. The map of activa- tion likelihood values can also serve as a source of independent coordinates for future region-of-interest anal- yses. We observed significant cortical activation probabilities in: bilateral anterior insula and overlying frontal operculum, bilateral mid dorsal insula and overlying Rolandic operculum, and bilateral posterior insula/parietal operculum/postcentral gyrus, left lateral orbitofrontal cortex (OFC), right medial OFC, pre- genual anterior cingulate cortex (prACC) and right mediodorsal thalamus. This analysis confirms the involvement of multiple cortical areas within insula and overlying operculum in gustatory processing and provides a functional ‘‘taste map’’ which can be used as an inclusive mask in the data analyses of future stud- ies. In light of this new analysis, we discuss human central processing of gustatory stimuli and identify topics where increased research effort is warranted. Hum Brain Mapp 32:2256–2266, 2011. VC 2011 Wiley Periodicals, Inc. Key words: activation likelihood estimation; functional brain imaging; fMRI; gustation; taste; PET r r Contract grant sponsor: National Institute on Deafness and other Communication Disorders (NIDCD); Contract grant number: INTRODUCTION R03DC009869; Contract grant sponsor: German Academic Exchange Service (DAAD). Taste stimulation has consistently activated the same *Correspondence to: Johan N. Lundstro¨m, Monell Chemical brain regions across multiple imaging studies [Faurion Senses Center, 3500 Market Street, Philadelphia, Pennsylvania et al., 2005; Small et al., 1999], activating the insula and 19104. E-mail: [email protected] overlying operculum, large portions of cortex. However, it Received for publication 3 March 2010; Revised 27 August 2010; is unlikely that these entire regions are taste-responsive. Accepted 13 September 2010 Small et al. [1999] have proposed in their review that there DOI: 10.1002/hbm.21188 may be multiple sub-areas within the insula and opercu- Published online 8 February 2011 in Wiley Online Library lum that process gustatory inputs. In the past decade, (wileyonlinelibrary.com). more reports of taste imaging have been published that VC 2011 Wiley Periodicals, Inc. r Identification of Human Gustatory Cortex r report activity in various areas in insula and operculum. hypothalamus, hippocampus, and striatum [Cavada et al., However, disagreement across studies in the precise loca- 2000]. tion of these subareas makes their identification difficult. Many of the regions that contain taste-responsive cells In this study, we conducted a meta-analysis of 15 peer- are remarkably heteromodal (or multi-sensory), containing reviewed studies using activation likelihood estimation only a small portion of cells that respond to taste stimuli (ALE) to identify which brain areas are activated by taste in primates: 6–27% in insula and overlying operculum solutions with a high probability. ALE gives a quantitative [Hirata et al., 2005; Scott and Plata-Salaman, 1999], 20% in estimate of activation based on coordinates of foci reported caudomedial OFC [Pritchard et al., 2005], 1.6% in prege- in each study. Each focus is weighted for the number of nual ACC [Rolls, 2008b], and 2–8% in caudolateral OFC subjects participating in the study. The resulting ALE [Rolls et al., 1990]. This differs from the responsiveness of value is submitted to formal statistics and corrected for sensory cortex cells for other modalities, which are mostly the observation of false positives. Through the use of ALE unimodal in that a majority of neurons respond to stimula- we identified brain sub-regions that are reliably activated tion from the principal modality; for example, 99% of by taste stimuli across studies. neurons in primary auditory cortex respond to tones [Phil- lips and Irvine, 1981]. As such, the cellular representation of taste processing in the primate brain can be character- ized as both distributed and sparse [Scott and Plata-Sala- Anatomy and Neurophysiology of the Primate man, 1999]. Gustatory System Sensations of taste, which are qualitatively labeled as Human Clinical and Neuroimaging Studies sweet, salty, sour, bitter, or savory, originate from mole- cules interacting with taste receptor cells and presynaptic Early studies with patients confirmed the involvement cells within taste buds in the oral cavity [Chandrashekar of the insula and overlying operculum, and amygdala in et al., 2006; Tomchik et al., 2007]. The taste signals are con- gustatory representation in the human brain. Electrical veyed to the brain via branches of the facial (CN VII), stimulation of brain tissue in the insula and overlying glossopharyngeal (CN IX), and vagus (CN X) nerves to the operculum, amygdala, and hippocampus in patients with nucleus tractus solitarius (NTS), the first gustatory relay in epilepsy led to (mostly unpleasant) gustatory sensations, the brainstem [Witt et al., 2003]. In primates, second-order [Hausser-Hauw and Bancaud, 1987; Penfield and Faulk, gustatory fibers ascend from the NTS to project directly to 1955]. Lesions in the amygdala (as a result of stroke or the ventroposteromedial (VPMpc) nucleus of the thalamus resection for the treatment of epilepsy) led to changes in [Beckstead et al., 1980; Cavada et al., 2000]. From VPMpc taste recognition and intensity perception [Henkin et al., thalamus there are two main projections. The primary and 1977; Small et al., 1997b, 2001b,c, 2005]. Damage to the larger projection is located in an anterior region of insula insula and operculum resulted in impaired taste identifica- and overlying frontal operculum (AIFO) and extends ros- tion and discrimination, as well as changes in intensity trally into the lateral orbitofrontal cortex (lOFC) [Mufson perception [Bo¨rnstein, 1940a,b; Cereda et al., 2002; Mak and Mesulam, 1984; Ogawa et al., 1985; Pritchard et al., et al., 2005; Pritchard et al., 1999; Stevenson et al., 2008]. 1986]. A second, less extensive, primate thalamic projec- Although the damage often encompasses large portions of tion terminates in the precentral extension of Brodmann the brain, the variation in locations across patients in these Area 3, along the ventral part of the precentral gyrus in studies confirms the extensive representation of gustation primate [Ogawa, 1994; Pritchard et al., 1986]. Thus, ana- in a distributed network in human cortex, involving the tomically, there are two ‘‘primary’’ thalamo-cortical gusta- insula and the overlying operculum. tory projections; in terms of anterior/posterior orientation, Taste neuroimaging studies commonly report activations one would be located anteriorly and one in a more mid- throughout the insula and overlying operculum, including: dle/posterior region of the insula/operculum area. How- anterior insula and overlying frontal operculum, mid ever, the latter’s existence and exact location is insula at the base of the precentral sulcus and overlying controversial and relatively little is known about gustatory Rolandic operculum, and posterior insula and overlying coding in this area (but see [Hirata et al., 2005]. Signals parietal operculum—the latter frequently extending into from the AIFO project to medial orbitofrontal cortex postcentral gyrus [Barry et al., 2001; Bender et al., 2009; (mOFC) and lOFC [Baylis et al., 1995; Carmichael and Cerf-Ducastel and Murphy, 2001; De Araujo et al., 2003b; Price, 1995; Pritchard et al., 2005], and the amygdala Faurion et al., 1999; Grabenhorst et al., 2008; Haase et al., [Aggleton et al., 1980; Mufson et al., 1981]. The pregenual 2007, 2009; Kinomura et al., 1994; Kobayakawa et al., 1999; cingulate cortex (prACC) is connected to the thalamus, McCabe and Rolls, 2007; Mizoguchi et al., 2002; O’Doherty insula, and the OFC [Carmichael and Price, 1996; Vogt et al., 2001, 2002; Veldhuizen et al., 2007]. Activations of et al., 1987], and recently taste responsive neurons have medial and lateral OFC are also frequently observed in been identified in the macaque prACC [Rolls, 2008b]. Fur- response to gustatory stimulation [De Araujo et al., 2003b; ther areas that connect to the macaque’s
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