B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6

a v a i l a b l e a t w w w. s c i e n c e d i r e c t . c o m

w w w. e l s e v i e r. c o m / l o c a t e / b r a i n r e s r e v

Review

The neurocognitive bases of human multimodal food perception: Consciousness
Justus V. Verhagen⁎
Dept. Biology, Boston University, 5 Cummington St, Boston, MA 02215, USA

A R T I C LE I N FO Article history: Accepted 6 September 2006 Available online 6 October 2006 Keywords: Taste Gustation Smell Olfaction Somatosensory Chemesthesis Flavor Recurrent network Perirhinal cortex Insular cortex Orbitofrontal cortex Amygdala Food Multisensory integration Affect Attention Perception Consciousness

AB S T R A C T 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 flavorsensory 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 nonoral 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. © 2006 Elsevier B.V. All rights reserved.

⁎ Fax: +1 617 358 1124. E-mail address: verhagen@bu.edu. 0165-0173/$ – see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.brainresrev.2006.09.002

. . . amygdala AI/FO. . piriform cortex (also called pyriform. . . . . . . . . . . . . . . . . . . . . Basic notions . . . . main olfactory bulb NaCl. . . . . . . . . . . . Conscious experience . . . . . . . . . .1. . . . . . .2. . . . . 2. . olfactory bulb OFC. . olfactory receptors PBN. . . . . . . cranial nerve cNTS. . . homeostatic interoceptive system I. . . . granular insula IT. . . .2. . . . . inferotemporal cortex LGN. . . . . . The neural correlates of flavor experience. . . . . . anterior cingulate cortex Ag. . . . agranular insula Id. . . . . . . orbitofrontal cortex oHIS. . . . . . . . . 2. . . nucleus of the solitary tract OB. . . . . . . . . . . . . . posterior piriform cortex PPC. . . . . chorda tympani DMV. . . . . . . . . . . . . . . . 2. . . ventroposteromedial nucleus of the thalamus VPMpc. . non-oral part of the homeostatic interoceptive system NTS. . . . perirhinal cortex (BA 35. . . . . . . motor trigeminal nucleus MOB. . . . . . spinal trigeminal nucleus STS. . anterior insula/frontal operculum CN. . . . rostral nucleus of the solitary tract spN5. .2. . . . superior temporal sulcus TEO. 273 274 274 275 275 275 . . . . . . . Conceptual background . . . . . . . lateral geniculate nucleus LOT. . prepyriform. 36) rNTS. dorsal vagus motor nucleus ErC. . .1. . . . parvicellular part of the ventroposteromedial nucleus of the thalamus Contents 1.2. . dysgranular insula Ig. . . . . . . . . . sodium chloride noHIS. . . . temporal-occipital area VPM. . . . . lateral olactory tract mN5. . . . . . posterior parietal cortex PrC. centiPoise CT. . . . . . . . . . . . . . . The homeostatic interoceptive system . . . .272 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 Abbreviations: ACC. . . . . primary olfactory or olfactory paleocortex) pPC. . . . . . . . . . . . 2. . . . . . . . parabrachial nucleus PC. insula Ia. . . . . . . Introduction and basic anatomy . 2. frontal operculum HIS. entorhinal cortex (BA 28) FO. . . . . . . . caudal nucleus of the solitary tract cP. oral part of the homeostatic interoceptive system ors. . . . . . . . . .

. . . . . PC: piriform cortex. . Ig/FO: granular Insula/Frontal Operculum. . ACC: anterior cingulate cortex. . . . . r/lIa: rostral/lateral Ia. . . which allows parallels to be drawn with prior work on awareness that is not considered to be flavor-related (Section 2. . . . . . . . . . . . . . . A schematic diagram of the ascending sensory systems contributing to flavor perception is provided in Fig. . . . . . . . . . .2). . . PrC: perirhinal cortex. . . . Mesulam (2000). Based on the concepts borrowed from the literature on visual consciousness. . . . 2 and 3. . . . . . Ia: agranular Insula. . . . . . the potential roles of flavor-related neural structures in flavor awareness are outlined next (Section 2. . awareness . . . spN5: spinal nucleus of CN5. . . . . . . 2. . . . . . . . (2000). . . . . . the reader is introduced to the current consensus on neural correlates of awareness as based largely on the visual sciences (Sections 2. . . . . . . . Recurrent activation. . VPM(pc): (parvocellular part of the) ventroposteromedial nucleus of the thalamus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .4.2. . . . 1 are the striate and extrastriate areas of the ventral “what” system (Van Essen and De Yoe. . .5. . . . 1996).B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 273 . . . . . . . and object . where it is also argued that object and affect awareness are served by separate yet overlapping cortical areas. . . c: caudal).3. yet all of them based on the visual neurosciences. . . . 3. .2. . 1. . . . G1. . . Barbas (1993). Acknowledgments. . . . . . . . Essential nodes . . . . . .2. Abbreviations (in order of appearance): LGN: lateral geniculate nucleus. . . . . . . . . . . Next. . . . TE/TEO: temporal (-occipital) visual areas. References . OFC: orbitofrontal cortex. . . Sewards and Sewards (2001). . Based on Norgren (1984). It is the aim of this review to layout parallel concepts. . The perirhinal cortex. . affect 2. . ErC: entorhinal cortex. 2 and 4. . . . . Attention. . 1995. . 2. . . MGN: medial geniculate nucleus. .2. . . . . V1. Id: dysgranular Insula. . . . . . . S1 and S2: somatosensory areas 1 and 2. 1 – Schematic diagram of ascending neural pathways contributing to food perception. . 1967. . . . NTS: nucleus of the solitary tract (r: rostral. . Several structures are omitted for simplicity. . 2002).2. . . . . . . . . . . . . . . . . DCN: dorsal cochlear nucleus. 1. A1 and A2: auditory areas 1 and 2. . . . . Brodmann's numerical labels indicated where known. . . . Rolls and Deco. .2. . . . . . . . . . . . . . . . . .2. . . . . . . .5) and attention is discussed last. . Visual IT projects to amygdala (Ag). . . . .4–2. . . Rolls and Baylis (1994). . . . the gustatory system is described as a homeostatic interoceptive system.1 and 2. . . . . . . . . . . . .2. . . mN5: motor nucleus of CN5. V2 and V4: visual areas 1. After a general overview of the anatomy of neural sensory systems (Section 1).1). . . The visual system contributes to food perception mainly in the distal recognition and selection of food (Pangborn. Heimer (1994). . . . . . . .2. Moving from striate primary visual cortex (V1) to inferotemporal TEO and TE visual receptive field sizes increase and optimal stimuli become increasingly complex. . . . IC: inferior colliculus. . . . G2 and G3: gustatory areas 1. . Introduction and basic anatomy The neural basis of consciousness has become a topic of great interest during the last decade. . . . Cardello. HF: hippocampal formation. . . . . . .3). . . . . . . . . . . . . . . . . the concepts of essential nodes and recurrent activation are applied to the flavor neurocircuits (Sections 2. . Conclusions. Following the visual literature. SOC: superior olivary complex (non-obligatory relay). . . . OB: olfactory bulb. . . . . . . . but for the field of flavor neuroscience where such ideas have not yet emerged. orbitofrontal cortex (OFC) and nearby perirhinal cortex (PrC) Fig. . . Several intriguing ideas have been proposed. . . . . Ag: amygdala. . . 277 282 282 283 283 284 284 2. . . . . . Most sensory systems of humans are involved with the perception of food.6. . Cavada et al. . . . Indicated in Fig. Craig (2002). .

Di Lorenzo. 2003). 1999. ultimately giving rise to a reverberating neural net standing wave among these structures. psychophysics (Doty and Laing. neural coding in primates (Scott and Plata-Salaman. which projects to A1 and A2. Reviews are available on olfactory transduction (Buck. 2006). also know as the hard problem of consciousness. 2000). Contreras and Lundy. Here we are concerned only with the specific consciousness (awareness) of experience.and dermatopic). 2003. 2003). Scott and Verhagen. Baylis et al. Conscious experience Conceptual background Several global stages of awareness have been described. which projects. 2001). 2000). Crick and Koch (2003) have been influential in this area and below I will outline their framework and compare it to work of others (see also Rees et al.1.. The nature of the neural codes in these systems may be spatial and/or temporal. 2. periodontal receptors and deep cutaneous receptors and projects to S2 (the lateral sulcus and insula (I)) (p. Golgi tendon organs. 2000). though not all suggest that multimodal cortex is part of it. synchrony. The proprioceptive system aids in the identification of texture. Dehaene et al. 1996). Grossberg (1995) employs the term “adaptive resonance”. Verhagen and Engelen. The oral input to the gustatory system arrives by way of cranial nerve 7 (facial). Rolls and Scott. psychophysics (Schiffman. 1992. 2002. Scott and Plata-Salaman. A2 projects to OFC and adjacent PrC (Murray and Bussey. John. called qualia. 2000. δ-power. neural coding in primates (Buck. Savic. which in primates directly projects to the parvicellular part of the ventroposteromedial nucleus of the thalamus (VPMpc). 2001). 2001). These nerves converge in the rostral NTS. (2003) suggest that neural structures of the “global workspace” (any combination of multimodal areas of the cerebral cortex. Erickson. allowing for the phenomenon of mixed gustatory– somatosensory sensitivity of neurons at the level of the rNTS (Norgren. Llinas and Ribary (2001) speak of “thalamocortical resonance” and Engel and Singer (2001) of “temporal binding”. ranging from coma to alert (Zeman. 1999. correlated firing. They propose that a conscious percept is related to a transduced stimulus being propagated through the vast neural networks of sensory systems to finally activate the (pre)frontal cortex. Due to space constraints. neural coding in non-primates (Laurent. 9 (glossopharyngeal) and 10 (vagus). 1984. 2000. 1994). see Fig. by way of the motor part of the trigeminal nucleus (mN5) and the ventroposteromedial nucleus of the thalamus (VPM) is represented in Brodmann's area 3a (part of S1). CN5 and 9 also project to the rostral NTS (rNTS). Controversy remains on which of the various measured neurophysiological activities (e. and involve labeled-lines. depending on the sensory system. involved with the milieu exterieur.” a more agreeable starting point than investigating causal relationships. Rolls and Deco. Those involved with gustation and visceroception are classed as paralimbic heteromodal cortex. proprioception and somatosensation belong to the class of unimodal isocortex. Gilbertson and Margolskee. Haberly.. The dorsal “where” system has been omitted for simplicity. From there back projections feed back onto previously activated structures of the sensory systems. The notion of such reverberation has been suggested by several authors. tono. in which processing occurs simultaneously at various hierarchical stages mediated by back-projections at every stage in the hierarchy (Hudspeth and Logothetis. audition. 1994). OB projects to the pyriform cortex. like the prefrontal cortex) send diffuse backprojections to prior sensory structures. Smith and St. 2000. auditory and somatosensory cortex show a topographical (retino-. 2002). Moon and Ronnett. 2003). 1996. Edelman (2003) has used the term “reentrant processing/signaling” for such reverberating network activation. 2000.g. 1996). 2000. Sobel et al. 210 in Heimer.. Firestein. and neural imaging (Small et al.. Current investigations are limited to identifying the “neural correlates of consciousness. Smith and Scott. and on whether the substrate is cortical or not (Hudspeth and Logothetis. via the VPM. 1999. Similarly. Smith et al. γ-power) relate most to conscious experience (see . The auditory system plays a role in the sound of chewing or biting food. 2000). I shall only refer to reviews pertaining to the gustatory and olfactory system in isolation. Neuroscientific experimental research in this field has only begun during the last few years. The visual and auditory system have a parallel hierarchical organization. The cortical areas involved with the processing of vision. Cleland and Linster. Sound is transduced in the spiral cochlear nucleus. Olfactory receptor neurons specifically converge on the mitral cells in the glomeruli of the olfactory bulb (OB) via cranial nerve 1 (olfactory nerve). 2001. The cranial nerves 5 (trigeminal) and 9 (glossopharyngeal) provide somatosensory input from the oral and nasal cavity to the spinal trigeminal nucleus (spN5). These modules are context-dependent dynamic entities having non-classical receptive field properties which can be modified continuously by experience through synaptic plasticity (Hudspeth and Logothetis. sparse coding or across-fiber patterns. 1996. which projects to agranular Insula (Ia). Primary cortical areas of the visual. They are multimodal in nature and closely related to the milieu interieur (Mesulam. 2000). Scott and Giza. 1994). Extensive reviews are available on gustatory transduction (Lindemann. 1999. 2001.274 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 (Van Essen and De Yoe. 1996. projecting to several brainstem nuclei via CN 8. neural coding in non-primates (Scott. Lamme and Roelfsema (2000) argue that recurrent interactions are necessary for awareness (for a graphical depiction of this process. modular. 2000. 2003. including mastication and tongue movements (Cardello. via activation of muscle spindles. 2. 2003). 1995. 1991. 1 there). 2000). and neural imaging (Zald and Pardo. Wilson and Sullivan.. OFC and entorhinal cortex (ErC) (Zald and Pardo. 1983). organization which may imply local neural processing. 2000. 2002). Proprioceptive information. The VPMpc in turn projects to the anterior insular and opercular areas (AI/FO) which project to the orbitofrontal cortex (OFC) (Norgren. to the primary and secondary somatosensory cortex (S1 and S2) (Heimer. shape and size of foods via active oral exploration of the food. 2003). Murray and Richmond. 2003). Haberly.

and Fig. This area is considered to be involved with memory and learning. 2001). analogous to that of the ventral visual system (RGCs → LgN → V1 → V2 → V4 → IT) (Fig. No similar data are available for the orolfactory (i. Dehaene et al.2. perhaps in the form of sustained activation of a set of cortical modules (Crick and Koch. assuming rate coding. The homeostatic interoceptive system Roughly consistent with this framework. most (visual) conscious experience. Which cortical areas might provide such backprojections to the orolfactory system? This is analogous to the question of which areas provide the feedback putatively needed for the aforementioned reverb trail in IT. 2000). Thus. forced choice responses on test-stimulus identity were well above chance (∼ 75%). and consistent with the hypothesis of Crick and Koch (2003).g. which was reflected by the finding that human subjects were either conscious or not of the masked stimulus in a similar task. Crick and Koch further suggest that this reverberation results in the selective and competitive activation of “essential nodes” (Zeki. In contrast to many other studies (Engel and Singer. and has been well characterized in terms of structure–function relationships. Intriguingly. They showed that a masking task would prevent the reverberating trail of activity due to diffuse backprojections from the global workspace.2. 2. 1. auditory and motor association cortices which are nested between high-order multimodal association cortex and their idiotypic primary sensory cortices which are related to deriving information from and manipulating the external milieu (Mesulam. these concepts are applied to the gustatory and olfactory system.11 in Mesulam.g. temporal and cingulate. 2004). 2000). Using the same task in human subjects. As the visual system is the most researched among the sensory systems. 2003. Engel and Singer. suggesting lack (or very incomplete) consciousness of stimuli despite reasonable (implicit) task performance.1. Rolls reported lack of synchrony in the visual system (IT) of awake macaques (Tovee and Rolls. Interestingly.2.. it will nevertheless be important to explore in which order such multimodal association cortices will become involved. for conscious experience) can readily be seen as consisting of the sequential activation of the neuraxis within each of the “classical” sensory systems (for example for gustatory stimuli: NTS → VPMpc → AI/FO → OFC. demonstrated that these measures may well be different aspects of the same underlying phenomenon. mediated via the hypothalamus. These areas are much more closely related to the internal milieu. 2 in Mesulam. 1). Damasio (1994) has proposed that awareness of the body-self is mediated via recursive meta-representations of homeostatic feelings. an area at the end of the dorsal visual object stream and analogous to human fusiform gyrus. which is insufficient. In summary. yet rated clarity of the stimuli was not. oral-sensory and olfactory) senses. the converging evidence of neurophysiological. it is equally plausible that this was due to back projections from cortical areas further downstream. amygdala. for olfactory stimuli: OB → Pyr → AI/FO → OFC).5. Rolls showed that there was a clear relationship between the amount of information available from IT and the apparent clarity/consciousness of the test stimuli. using a backward masking visual task (test stimulus before masking stimulus). In Sections 2. 1992). see Fig. a set of which is termed a ”coalition”. Dehaene et al.B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 275 e. 2. computational and behavioral studies reviewed very briefly here suggest that back projections (from association cortices) are correlated with. these downstream areas activate (multimodal) association cortex from which they will in turn receive (diffuse) backprojections allowing for sustained activation to develop in the network (note that within this period also horizontal and early backprojections may have become active). The neural correlates of flavor experience Basic notions It should be kept in mind that the olfactory and taste system (and more globally the OFC.2–2. employing a neurocomputational model. temporal pole. Though this ultimately may be true (as these higher association areas are highly interconnected). see also Fig. 2001). 2000. Incidentally. hippocampus) and high-order multimodal association cortex (see Figs. 2003). Insula.2. smell and pain (Mesulam. Despite lack of direct evidence. Though Rolls (2004) attributed this reverb trail to recurrent collateral projections within IT. It is proposed that we are conscious when coalitions engage in sustained activation. Rolls (2004) showed a reduction of what may constitute a reverb trail of activity of neurons in monkey inferotemporal cortex (IT. 2001). 2003).e. in that it was suggested that the information threshold is higher for conscious experience than for implicit task performance (Rolls. under the explicit assumption that the derivations based on the visual system will apply. The forward sweep (the initial processing stage. One task then is to extrapolate the framework to the orolfactory systems.. nested between limbic (pyriform cortex. though. 2. rhinal-cortex and parahippocampal region) can be considered to be part of the paralimbic (mesocortical) areas. cingulate cortex. than the unimodal visual. most of the aforementioned concepts have been derived from vision science. immune response and endocrine balance (homeostatically) to mental state and with the perception of taste. linking visceral state. At the next stage. channeling emotions and affiliative behaviors. (2003). when this period became similarly short (∼ 20ms). temperature hunger and . One answer may be that it is the general “global workspace” of highly interconnected multimodal association cortices (e. 1) as the masking stimulus was presented at increasingly shorter periods after the onset of the test stimulus. if not necessary for.2. 2000). as outlined below. there is no reason why the neural correlates of consciousness could not also be investigated there.. as delineated in his somatic-marker hypothesis.2. activation of AI/FO would activate excitatory neurons with long-distance axons which would project back onto AI/FO as well as to other high-level areas resulting in global brain scale states of activity (Dehaene et al. They further reported that in the network this reverb was likely to be either present or not. though necessary. 1998) that provides this feedback toward any sensory system. prefrontal.11a in Mesulam. 1−6 and ch 1. parietal. It is currently thought that the insula–OFC network represents such interoceptive bodily feelings as pain.

2001. sensory exposure to food and pure chemicals without ingestions leads to an early miniature version of postprandrial release of various digestive and metabolic components like saliva. 2005).. OFC: Kadohisa et al.b). De Araujo et al. This is very similar to imaging studies in taste (O'Doherty et al.. Small et al. 2002). Thus flavor appears to play a special role in evoking cephalic phase responses in humans. the gustatory and homeostatic interoceptive systems run largely parallel in close spatial association to each other from the NTS onward. 2002. 2005). 2006). The oral division of the homeostatic interoceptive system (oHIS) is proposed to represent the same modalities as the non-oral division (noHIS).. a glucose solution) are much less pronounced than in rodents. but form a separate system involving homeostasis and interoception (e. nociceptive and thermal input related to maintaining proper body function). 1996) sensitivity (cranial nerves: Rentmeister-Bryant and Green. thought to mediate pain. 1996. 1968. 1996).b. 1986) or when presented with whole foods (Teff. and primates rely more on cortical HIS than sub-primates (Craig...g. in part via PBN. 2003a. 1988). Chemesthetic stimuli have similar sensory effects on the skin as in the mouth.. PBN). In mammals. and nonoral part. Thus. just sight and smell of a food can lead to increased glucose clearance. in addition to the strong neuroanatomical similarities. 2002). 1986. 2004. This response is considered to be preparatory and to adaptively affect both metabolism and behavior (Teff. Feldman and Richardson. without swallowing. 1989. VMb) (Craig. 1999. nociceptive and visceral) system was also proposed by Katz et al. VPMpc: Pritchard et al.. Verhagen et al. for overview see Table 2 in Verhagen et al. as in rodents (e. OFC. but has not been previously associated with HIS. 1999. I thus suggest the terms oral common-chemical sense (oCCS. taste.. ACC and Ag (Francis et al.b. These modalities form the core of Craig's HIS modalities.. DMV is dorsal motor nucleus of the vagus). in the form of parasympathetic cephalic phase reflexes (Teff.. AI/FO: Scott and PlataSalaman.: Lundy and Contreras..276 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 thirst and is necessary for subjective feelings (Craig. Craig. Ogawa et al. The gustatory Ia is located just anterior to the Ia involving the homeostatic interoceptive system (Craig. This leads us to propose that the homeostatic interoceptive system consists of two major divisions: an oral part..g. 2005. 1993). 1983 for a related conceptual issue). which provide the advantage of conceptual simplicity. 1984. also known as the basal part of the ventromedial nucleus. Both systems are strongly involved with brainstem homeostatic nuclei (NTS. This neural system is very similar to that of the gustatory system. 2004. 1997. the sympathetic Lamina1 division provides the basis for the somato-autonomic reflex arcs at spinal. Ag: Kadohisa et al. 1989. The same has been shown for oral chemesthetic (Green..v. evolutionarily these systems (OHIS and noHIS) developed in parallel. 2003. The identified human neuraxis (Fig. On the other hand. Interestingly. 2003). it has been found that taste sensitive neurons also show sensitivity to touch and temperature (chorda tympani: Aato et al.. Craig notes that for sub-primates the PBN is an obligatory relay (Craig. results in a 33% lower postprandrial glucose levels (i.g.. Thus. including thirst. and the primate taste system is as directly involved with homeostatic regulation as the noHIS. intestine. 1988. Matsuo et al. 2002). whereas responses become more robust as the number of involved modalities increase (e. 2004. smell. Virtually all imaging studies related to these modalities on the skin show activation of at least several of the areas of I. Further. Arguments. 1996). Further. gastric acid. This also holds for rodents (chorda tympani: Ogawa et al. On one hand this was based on anatomical findings of lamina-1 dorsal horn thalamocortical projections. 2004). 2003. Craig et al. human imaging studies consistently showed activation of especially the anterior insula in feelings of the body. Last. 1996). VPMpc: Verhagen et al. a 5-min oral exposure to a sandwich. 2000) in rodents and also by Scott and colleagues (Scott and Mark. 1981. VMpo (posterior part of the ventromedial thalamic nucleus) is rostrally contiguous with the VPMpc (the parvicellular part of the ventroposteromedial nucleus. 1986). “visceroception”) for fine parasympathetic afferents involves NTS → VPMpc → Id → Ia → lIa. part of noHIS). Ag: Kadohisa et al. These exist in the gustatory system as well. linking it with Damasio's hypothesis and recent imaging studies. metaboreception. Small et al.. S2). primarily mediated via NTS→ DMV→ efferent vagus nerve to stomach.. in humans cephalic phase reflexes to simple stimuli (e. 2001. medullary and mesencephalic levels (see Fig 2 in Craig. They argued that these sensations are not so much related to somatosensation (and hence mediated via S1.. GC: Yamamoto et al. 2002). 1975. and for fine sympathetic afferents Lamina 1 → VMpo → Id → Ia → rIa → OFC (lIa: lateral Ia. injected glucose) (Teff. It provides the sensory link between . 1996).. especially as recently proposed by Sewards and Sewards (2001). (Katz et al. and both lamina 1 and NTS project to VPMpc.. 2004). with as a main difference (besides that of location) that the oHIS further contains an expanded representation of chemosensory sensitivity related to papillary oral input. 2003) (for a meta-analysis see Verhagen and Engelen. 1999. The reasons for this heteromodality make considerable sense in the context of HIS. rIa: rostral Ia) (Craig. 2005. 2002. 2003a. pain. 1. Note that the idea of the gustatory system as being part of a larger multimodal (gustatory. cranial n. OFC: Kadohisa et al.. part of oHIS) and non-oral CCS (noCCS. 2003a. in humans. 1999. NTS: Matsuo et al. In noHIS. AI/FO: Verhagen et al. 2002). The existence of a cortical system involved with homeostatic interoception has been proposed (Critchley et al. Kosar et al. vision. 1).g. In the following it is argued that taste is associated with interoception... cutaneous. who propose NTS → VPMpc → gI → dI → aI (Fig. Craig. 1995. supporting this proposal are as follows. It is known that the primate gustatory system is not unimodal: at every level of its neuraxis (from cranial nerves to Insula and OFC) that has been tested. as in the taste system (Norgren.. 2000).. skin temperature and sexual arousal (Critchley et al. itch and temperature (Craig. 2002. NTS: none tested. 2002). The human salivary and gastric response is correlated with the perceived pleasantness of foods and foods with high hedonic value will be metabolized more rapidly (Teff. the sense of taste itself is clearly related to homeostatic interoception. see Satinoff. Lamina 1 also projects to NTS.. pancreatic enzymes and insulin. Thus. Shimatani et al. liver and pancreas.

2004. The perirhinal cortex.07 ± 0. affect and object awareness The notion of the taste system as part of HIS suggests that awareness of taste may be mediated by means as envisioned by Damasio. including the insular cortex. Indeed.2. 1995). respectively. Below the concept of object versus affect awareness is introduced. This may suggest that conscious experience of these two aspects of food perception may involve overlapping but also discrete cortical areas. based largely on rodents. It has long before been proposed that rodents and primates differ substantially in this respect. top).. new analyses based on data from Rolls et al. 2003. functional. (2003). the identification of an intraoral food relates to the integrated perception of all concurrently stimulated modalities available.. I hence take Sewards proposal to only refer to sub-primates. 1985. Scott and PlataSalaman. 2. while largely ignoring the overwhelming evidence of involvement of OFC in affective processes (as in reward devaluation or association) and lack of effect of reward devaluation in lower neural areas (Yaxley et al. the latter indicating higher neural responses being associated with higher acceptability ratings.13. taste: alkaloids.201).1% in AI/FO and 11. The distribution for the clOFC appears bimodal. 2004. nearly half (39. the food-source or food-state (retronasal olfactory: e. Verhagen et al. 1. whereas they are encoded serially in primates (quality in AI/FO. In line with this.08) as evaluated with a 1-sided t-test (p < 10− 5and p < 10− 4. 2.16 ± 0. The notion of two separate systems for “object” (quality and intensity) identification versus affective evaluation has previously been suggested by Small et al. but did not differ between AI/FO and Ag (p = 0. 2005. I propose that the Insula–Perirhinal system functions as an orolfactory object recognition system. as indicated in Fig. 2000). This object-affect dichotomy is strengthened by a novel analysis of the distribution of the correlations between the mean single-unit responses to a large (n = 16–25) array of oral stimuli of neurons in AI/FO (n = 41). except for OFC in BK (77%)). salt. yet the rhinal cortex played no role there). These anatomical. but does not provide insight into how the neural structures of this system (or those associated with olfaction) are involved with bringing about consciousness. 1989) of the monkeys these neurons were recorded from of the same stimuli (Fig. He suggests that such functional divisions.0% for AI/FO.4. 58.3. at least sub-cortically).B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 277 milieu exterieur and interieur by allowing informed decisions as to what food is appropriate for the body to ingest and absorb (Scott and Verhagen. this correlation was highly significant (p < 0.6 and −0. clOFC (n = 53) and Ag (n = 44) in awake rhesus monkeys and the individual acceptability ratings (method described and neurally validated in Rolls et al.6%) the population of clOFC neurons had significant (p < 0. such is reflected in a more negative or positive correlation between neural responses and behavioral measures of hedonic evaluation. Scott and Rolls (in gustation: AI/FO and OFC. 2 (bottom). As expected. top.g.06 ± 0. peanut butter. in that indeed in rodent taste quality and affect are encoded in parallel.2 and 0. rotten. after which the neural structures and their interactions are discussed in context.g. and hence there is no such direct relevance to the olfactory system in Damasio's somatic marker hypothesis or the recent neuroimaging data on interoceptive bodily feelings. Prescott mentions Gibson's ecological view of perception. The distribution of AI/FO and Ag neurons peaked between −0.4% in Ag. Thus. lumpy. In relation to retronasal aromas as being perceptually associated with the oral cavity/taste. It should be noted that the anatomical relationship between noHIS and the olfactory system is less evident (Fig. The Pearson correlation coefficient between the neural and behavioral responses across the stimulus array was computed for each neuron. a larger fraction of the clOFC population had more positive and negative correlations than seen in AI/FO and Ag (Fig. He argues that the survival value of the orolfactory system lies in its ability to correctly identify foods by jointly identifying its nutrients (gustatory: e.. the hedonic ratings explained on average 16 ± 13% of the variance in OFC (maximally 42%). SPSS Inc. With respect to gustatory awareness. 1995) and Anderson et al. carbohydrates.. Anderson et al. mean ± SD) than in AI/FO (0. consistent with our proposal. hard.01) and the cumulative histogram of their p-values was consistently higher for clOFC than for AI/FO and Ag. Rolls et al.6% for Ag and 22. This notion is strengthened by a population-analysis based on the same data (see Table 1 and Fig. Sewards (2004) suggested different neural structures associated with sensory and hedonic awareness than proposed here. Thus. Scott et al. The assumption is that if neural encoding involves affective processing. with peaks at correlations between − 0. activity of clOFC neurons to oral stimuli is often related to the hedonic evaluation of these stimuli by rhesus macaques.1. whereas this was only 12. proteins). can be made at any level within the taste system.5% of clOFC neurons had correlations with associated p-values smaller than 0. chemesthesis: capsaicin). affect in OFC. Kadohisa et al. 1988. the proportion of variance explained (r2) was higher in clOFC (0. For example.08) and Ag (0. electrophysiological and conceptual considerations lead us to suggest the oHIS and noHIS concept. while this was only 13. slimy) and toxins (e. 2.4 and between 0.g.8%)..4 and 0. 2004). such division between sensory and hedonic aspects has previously been suggested by Aurell (in Sewards. Prescott (1999) has provided a similar object-based approach to food perception. amygdala and OFC) for each monkey (BO and BK) was quantified using multi-dimensional scaling in 2 dimensions (all explaining >90% of the stimulus correlations' variance.05) correlations between their individual responses and the acceptability ratings. analyzed with SPSS V12.. respectively).. volatiles perceived as floral. texture: thick. It should be noted that even though such strong associations were present in clOFC. whereas the Insula–OFC system functions as an orolfactory affective system. 1999).. The relation between this abstraction and the monkey's behavioral . 3). (in olfaction: OFC and amygdala. suggesting that hedonic evaluation is not the sole neural correlate of clOFC activity. which entails that the physiological origins of sensations are less important than that the sensations can be used for object identification. respectively. 2003. Scott et al. whereas this relation holds to a much lower extent for neurons in AI/FO and Ag.. Analogous to this scheme.). The representation of the stimuli in each area (AI/FO.6. For many clOFC neurons (20.

23] = 1.20] = 1.21] = 5.091 [1.0 ⁎ 10−04 BK MDS r 0. and no more than 21% in the AI/FO (20.217 [1. Significance levels are boldfaced if significant (α = 0.23] = 9. It should be noted that this is a valid approach as an MDS solution is rotation-invariant.930 119 0.1 0.9 3.571 [1.3 0.23] = 115.278 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 Fig.057 [1.9 ⁎ 10−10 11 0.201 [1. 3 for details) BO Hedonic Ins Max Max F p Max Max F p Max Max F p angle (°) r2 124 0.). .163 70 0.21] = 27.218 [1.550 [1.6 0. 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. except for Ag of BK (number of neurons = 5).770 Indicated are the angle (“max angle”) of the rotation of the MDS at which the r2 was maximal (“max r2”.1 0.20] = 5.2 ⁎ 10−05 179 0. acceptability of the stimuli.5 0.23] = 31. Ag = amygdala and OFC = orbitofrontal cortex) in two monkeys (BO and BK) explained by the three factors of behavioral oral stimulus acceptability (“Hedonic”).049 [1.274 Hedonic Viscosity Temperature MDS r2 Ag angle (°) r2 0. correlations of nearly half (39. 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).977 0.8 ⁎ 10−05 86 0.015 104 0.8 0. The acceptability rating explained as much as ∼50% of the variance only in the OFC in both monkeys.1 and 11.834 [1.21] = 7. and the associated F.0 1.9 1.21] = 17.251 [1.23] = 4.1 ⁎ 10−05 Temperature 79 0.4%. 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. Microsoft Corp. stimulus viscosity and stimulus temperature (see Fig.293 [1.045 102 0.05).5 0.8 0.051 [1. 62° in OFC of BO and 34° in OFC of BK). using the solver function in Excel 2003. appears bimodal.20] = 24. The r2 of each MDS solution is also presented (“MDS r2”). stimulus viscosity and stimulus temperature.21] = 2. respectively). It further appears that representations of viscosity and hedonic value (where both are significantly correlated with rotated MDS stimulus locations) are most orthagonalized in the OFC (angle-difference is 16° (140°–124°) in Ins of BO.164 [1.0 0.6%) of the OFC neurons were significant.025 92 0.005 51 0. in contrast to that of neurons from AI/FO and Ag. See text for validation of the analysis. were evaluated by rotating the MDS solutions and computing the Pearson correlation coefficient between the new stimulus location and acceptability rating in 10 steps in Excel.1%) or amaygdala (9.290 73 0. 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.028 8 0.23] = 5.21] = 1.910 OFC angle (°) r2 0. MDSs were based on > 20 neurons and > 20 stimuli.(“F”) and p-value (“p”) of the regression.6 4.927 2 Viscosity 140 0.5 7. The distribution of OFC neurons.574 [1.2 0.025 92 0.1%).456 [1. The associated proportion Table 1 – The maximum proportion of variance (r 2) of MDS stimulus location for three brain areas (Ins = insular cortex/ frontal operculum.310 0.

viscosity correlated highly with MDS stimulus position (see Table 1 for details). intermediate for I (r2 = 0. Importantly.B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 279 Fig. 10.) and behavioral acceptability ratings (“Hedo”). this figure provides a novel population-level analysis between the locations of stimuli on a 2-dimensional scale (MDS. Table 1 indicates the maximum r2 obtained by rotation for each of the factors. again. inversion and translation. 3 – To complement the individual neuronal-level analysis of Fig. 3 as a function of angle of MDS rotation.201) and. SPSS Inc. and F. Note that rotation of the MDS. this population analysis suggests that the relation between populationencoding and hedonic value of stimuli is strongest in the OFC for both monkeys (proportion of variance explained is ∼50%). weakest in Ag . yields equivalent MDS solutions. only at the level of the OFC did the behavioral acceptability of stimuli (measured and analyzed separately for each monkey) correlate highly with the neural representation of the stimuli. Systat v. and additionally between these locations and stimulus viscosity (“Visco”) and stimulus temperature (“Temp”). In all three neural areas of monkey BO. Consistent with the above analysis based on these same individual neurons. 2. 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. as well as the associated angle. of variance explained (r2) is indicated in Fig. 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 acceptability data were available for insula in monkey BK). a means to visualize neural population representation of stimuli. as well as scaling.and p-value of their regression analysis. brain areas and subjects.

the PrC has been found to be necessary for crossmodal association memory.4. − 10. Fifth. Murray and Richmond. without a tendency to improve.201. Schultz et al. respectively. It has reciprocal connections with a vast number of cortical areas: insular cortex.012).9.099 ± 0. as well as olfactory bulb input). as they did not test flavor discrimination abilities (which is what our model would predict). −15. Sewards and Sewards (2001) suggest that the perirhinal cortex is a final common pathway for the visual. In conclusion. auditory and somatosensory systems.001) above control.3. and it is hence exceedingly unlikely that the values are assigned to the stimuli they actually belong to.4 SDs (p < 0. from 7 studies) when searching within an 11mm cube of the peak coordinates of the 296 individual activations. 2001).. 2006). Evidence has been presented in several reviews that the PrC. 1999.4. lesions to this area result in taste recognition deficits. 4 activations being the same as for BA 35. the auditory superior temporal gyrus and the gustatory posterior agranular insular cortex are all adjacent to the perirhinal cortex. parahippocampal complex (see Refs 13–15 in Murray and Richmond. odor study 11: 18. and is part of the temporal cortex that has been suggested to be one of the four multimodal cortices necessary for conscious experience via feedback (Dehaene et al. Third. Limiting the search to a 5 mm cube resulted in four identifications of BA 35 (taste study 2: 19. which is functionally and spatially closely associated with PrC and hippocampus (Verhagen and Engelen. This analysis confirmed that the reported maximum r2 values are highly unlikely to occur by chance: the mean (±SD) of the maximum r2 between randomly reshuffled hedonic ratings and rotated MDS of insular neurons in the insula in BO was 0. Note that for 24 stimuli the number of permutations of randomly assigned values is 6. −21 and −21. 2001). −4. 2006)).and z-coordinates. respectively) and left cluster 5 (−21. they could not rule out the possibility of “flavor blindness”. STS (auditory). and that this may hold for the gustatory system as well. providing the necessary connections for such multimodal input (and output). For the OFC. Monkeys with rhinal cortical lesions are unable to select visible objects that were selectively and arbitrarily assigned to either a peanut or a sultana which three monkeys orally sampled in full darkness (Parker and Gaffan.9. y = −20mm (−10 to − 40) and z = −12mm (−8 to −32) according to the map by Talairach and Tournoux (1988). According to the map by Talairach and Tournoux (1988).056. and 62° (monkey BO: 73°–11°) and 34° (monkey BK: 104°–70°) in OFC (Table 1).8 SDs (p ≪ 0. −14. In the Ag of OB. is important in object recognition (Murray and Bussey. Indeed. These coordinates overlap with right cluster 10 (18. The PrC represents an object's many (multimodal) attributes. PrC is not an unlikely candidate to be activated by odor and/or taste stimuli. the PrC has no role in . −15. To validate this novel method of analysis. Indeed. 2006) also suggests activation of PrC. where the actual data (r2 = 0. This analysis further suggests that the representation of hedonic value and viscosity (where correlations are significant) is most orthagonalized at the level of the OFC: the differences between the angles at which their correlations are maximal are 16° in AI/FO (140°–124°). amygdala. −7. −18. the tertiary gustatory cortex (Ia) is known to have reciprocal connections with the perirhinal cortex (Refs.090 ± 0. Deficits in a food preference task were not apparent in one of the monkeys (and in none of those with specific perirhinal lesions in the study of Gaffan. This too is consistent with our model. − 13. each of these four activations was located in BA 28 (ErC).3 SDs higher (p < 0. Although the authors argue that the deficit was due to a loss of flavor-vision association memory. the perirhinal cortex is generally believed to be important for object recognition in all other sensory modalities.and z-coordinates. the PrC associates different views and non-visual attributes (like touch or smell) mediating object identification. although the authors refer to it as amygdala and hippocampus. 2006). and hence predicted to be dissociable from the identification (Ia-PrC) system. cingulate cortex. hippocampal formation. from 8 studies) and BA 36 7 times (5 taste and 2 odor. y. Second.001) above control (0.1.7. x-. 2006) but never BA 36. Our cluster analysis-based meta-analysis of odor and taste neuroimaging (Verhagen and Engelen. x-. the insular secondary and tertiary taste cortices as proposed above project to perirhinal cortex. 2001).076). as well as cross-modal memory of objects and events (see below). the perirhinal cortex may provide the feedback to Ia which I suggest to be necessary for conscious experience/recognition of food as objects in a multimodal fashion. parahippocampal gyrus (near the perirhinal cortex. encoded in the affective system (the neural correlates have been found in the OFC. 2001). For example. whereas the maximum r2 for the actual ratings (0. Talairach Daemon found BA 35 11 times (5 taste and 6 odor.4. odor study 7: −22. 2001).074 ± 0. Even after 500 trials the mean error rate was 232 (not above chance level).280 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 (<10%). They present five arguments why the perirhinal cortex is the “terminus” of the taste system. y. as well as enthorhinal cortex (which receives strong pyriform input. Thus. OFC. the somatosensory posterior insular cortex. in that food preference is a function of relative hedonic value of foods.. − 5. It hence is clear that the analysis is unlikely to suggest strong relationships by chance.834) was 9. despite inability to perform the association task. It will be of considerable interest to further investigate the involvement of PrC and ErC in orolfactory neural processes. these analyses substantiate the notion that cortical and subcortical structures in primates are to different degrees involved with representing affective information. The PrC (BA 35 and 36) is located around x = ±20mm (range ±17 to ± 25). the randomized control analysis revealed a mean r2 of 0. − 12. 13.105. in IT) has been shown to be activated in human imaging studies (Sewards and Sewards. I randomly assigned the acceptance ratings and viscosity levels to the stimuli and performed the same maximalization-of-r2-byrotation analysis 20 times for each monkey. Indeed. area and factor. the very high r2 for viscosity (0. while recognizing that it remains an entity. 37 and 95 in Sewards and Sewards. 1994). see Table 1A in Verhagen and Engelen. 2003). 2000). located at the ventromedial surface of the temporal lobe. Fourth.456) were 3. somatosensory and auditory systems.2 ⁎ 1023. −23. within the typical range of variation of neuroimaging studies (see Verhagen and Engelen. see Table 1) was 2. it is the highest order area for the visual. the end of the dorsal visual system (TE). TE and TEO (vision). Interestingly. Thus. 1998). First. Table 2B in (Verhagen and Engelen. in that lesioned monkeys cannot choose a visible object first sampled by touch (Goulet and Murray.

Human imaging studies provide evidence for this as well. are reciprocally connected to each other. The amygdala and OFC. receiving input from paralimbic areas. Thus it seems plausible that AI is also involved with orolfactory affect in humans. 33 and 34 in Murray and Richmond. Critchley et al.. though to a lesser Fig. These findings lend further support for the neural basis of the orolfaction model proposed here. has dense reciprocal connections with the OFC (notably the medial OFC). OFC: orbitofrontal cortex. which. I argue that the same may hold for the gustatory system. 2001). Murray and Bussey (1999). and that is not related to (food) object reward associations (which I propose is mediated by the aI-OFC-Ag-ACC network. Only the olfactory and gustatory (oHIS: oral division of the homeostatic interoceptive system) systems are shown for simplicity. 4. Ag: amygdala. 2003). in a Gestalt-like fashion (Murray and Bussey. However. but overlapping. given that they may all be reciprocally interconnected. in that the PrC is critically involved with multimodal (food) object representations. I propose that two different. 41 and 42 in Murray and Richmond. has recently been implicated in representing the visceral self (Craig.. 1994). happiness (Critchley et al. that direct. Sewards and Sewards (2001).B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 281 object–reward associations. all areas speculated here to be involved with conscious experience via reverberation are considered by Mesulam (2000) to be “neural epicenters” in his model of largescale neural networks. PrC: perirhinal cortex. see Verhagen and Engelen. the right anterior insula (rAI). Id: dysgranular Insula. and hence perception. (2000). extent than OFC. PC: piriform cortex. Murray and Richmond (2001). In parallel. Combinations of epicenters may be dynamically formed in relation to the cognitive task at hand (for example the limbic large scale network for memory and emotion. in explicit subjective awareness and in emotion. Such epicenters (or “transmodal areas”) which are higher multimodal association areas. see also Kringelbach. whereas the OFC and amygdala are crucially involved in such associations (Refs. Furthermore. 2004. This hypothesis could be investigated with cellbody-specific lesions of the PrC on orolfactory food discrimination. intraprimate species differences should not be excluded. 4 – Proposed model of neural structures involved with the conscious experience of food. in that it is not necessary for reward devaluations (Thornton et al. and have been found with respect to prevalence of spindle cells which exclusively occur in these areas (see Ref. 2002. 2004) and disgust (Wicker et al.. the rAI becomes activated during various emotions as anger. For example. It should be noted. and its direct connections with OB are not shown for clarity. 2004).. 2001). Partially based on Barbas (1993). EnP: endopyriform nucleus. another multimodal cortex tentatively involved with such feedback. For example. MOB: main olfactory bulb. reported effects of eating chocolate to satiety on the insula and OFC in a human imaging study (Small et al. 2006) is similarly involved with affective awareness of food. part of noHIS. I speculate that these areas may be necessary for the conscious perception of the affect-awareness of food. Entorhinal cortex is incorporated in HF. is similar to Dehaene's global work space model mentioned earlier. specific evidence for a role for PrC in flavor processing remains absent. The PrC has further been shown to be important for discriminating visual features. This hypothesis is a modification of the exclusive involvement of the OFC among cortical areas in orolfactory affect as proposed by Rolls (1999) and has been incorporated in Fig. Indeed. Ia: agranular Insula. however. Rolls (1999). VPMpc: parvocellular part of the ventroposteromedial nucleus of the thalamus. the anterior cingulate cortex. 1999). These ideas are represented in Fig. large-scale networks are involved for (1) food object recognition awareness (Ia. may also be critically involved with affect awareness. consisting of the hippocampo-enthorhinal complex and amygdala as two interconnected epicenters. ACC and Ag). 29. which is the core of the somatic marker theory (Damasio. Mesulam (2000) suggests that the epicenters are also crucially involved with consciousness. 1998). or: olfactory receptors. which have extensive reciprocal connections. NTS: nucleus of the solitary tract. Ig/FO: granular Insula/Frontal Operculum. 2001). Abbreviations: gr: gustatory receptors. 2004) and as part of the IOFC-ACC system. PrC and Ag) and (2) food reward value awareness (Ia.. in that the oral part of the aI (also with a bias towards the right hemisphere. 4. ACC: anterior cingulate cortex. Cavada et al. Small et al. 22 in Craig. 2004). in humans and monkeys (Refs. OFC. . HF: hippocampal formation. which is based on the above considerations of the gustatory system being effectively the oral part of HIS. the hypothalamus and limbic thalamus). and receive reciprocal connections from many more lower order cortical areas and ultimately from the thalamus.

reported well-defined patches of labeled neurons in the aPC (Zou et al. Rolls et al.. and indeed reciprocal connections exist between PFC and OB in rat and it has been found that orbitofrontal regions can activate and inhibit the OB in rat (Cinellar et al.. 2003).2. reflecting reward versus punishment (Kringelbach and Rolls. in absence of clear functional maps for gustation and oral somatosensation in Ia.2.5. but to another taste in another subject. Scott and Plata-Salaman (1999) have found no clear evidence for modularity in the macaque AI/FO. Based on this evidence. Further. we may ask which neural substrates in the orolfactory systems could act as the tentative essential nodes? In the visual. as well as with different sensitivity to different modalities. In contrast.g. nor using 2-deoxyglucose and optical imaging in rat PC (Cattarelli et al. Thus. This spatial organization is thus lost postsynaptically. 2001)... this system is intimately involved in information processing” (Haberly. modular) organization.” pertaining to activity of neural areas related to processing of particular features (e.. rather than stimulus features.282 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 In conclusion. The necessity of feedback mediated reverberation has been questioned by Zeki (2001). but to be actively involved in its reconstruction.g. 2004). TE and TEO for complex configural object representation). hedonics) and Ia-PrC (food identity). 2. 2003). despite its inhibitory action on mitral tufted cells.. 2004. Differential. OFC or amygdala (Rolls et al. 2004. TMS) of higher order cortex (PrC. At this point. Alternatively. hemodynamic activations to five prototypical tastants of same intensity of this area were stable between imaging sessions within subjects. 2004). as well as the amygdala (affect and identity) in humans.. 2005).b. inspection of maps of reconstructed positions of responding neurons has not revealed any organizing principle related to modality sensitivity in either AI/FO. 2004). Indeed such a gradient may be sufficient to encode both the magnitude and value of the reward. Essential nodes With respect to the subsequent stage in the framework of consciousness. The second identified functional axis (anterior–posterior) was suggested to be related to the level of abstraction of the stimulus or task. 2004). MT motion coding).. auditory and somatosensory system. each within a cortical area with clearly defined properties needed for explicit awareness of that property (e. a recent human neuroimaging study of the insular/opercular cortex has suggested gustatory chemotopy (Schoenfeld et al.4. 2003). Recurrent activation A more fundamental question is whether recurrent activation occurs at all in AI/FO. Haberly states that “the exceedingly large number of backprojecting pyramidal cell axons from aPC (much larger than in the LOT) suggests that. Kadohisa et al.. Experiments employing techniques such as temporal lesions (cooling. Backprojections from the anterior piriform cortex (aPC) to the OB have also been identified in rodents (Haberly.g. and to reduce the ability/speed to recognize food and modulate its pleasantness. in order to acquire knowledge. for olfaction essential nodes may consist of (groups of) glomeruli. 2003. employing single olfactory receptor clones. yet overlapping. Further. This is presented in a context where the brain is not so much thought to merely represent reality out there. More work on the functional organization of higher cortex of the orolfactory systems seems warranted. 2. 2003a. 2001) large-scale network is involved. With respect to the proposed neural structures involved with food object awareness. This may indicate that the preferential reverberation between PrC and a subregion within Ia may consistently be related to awareness of a salty food in one subject. Mountcastle. no discrete spatial odorant activations have been found in the PC in rats using c-fos technique (Illig and Haberly.. due to overlapping input to the aPC (for example odorants can activate multiple olfactory receptors) and due to associational fibers (Illig and Haberly. I present evidence that the neural circuitry involved with object versus affect awareness of flavor is both overlapping and distinct. A genetic tracer study. three synapses upstream from the Ia). With respect to the proposed food affect awareness. a recent optical imaging study of rat gustatory cortex has indicated an anterior–posterior map reflecting responsiveness to sucrose or NaCl (Yoshimura et al. 1987). such modularity and larger scale cortical functional divisions do not appear to exist at higher cortical levels for the orolfactory systems (Ia-PrC for orolfactory object awareness and Ia/OFC for orolfactory affect awareness). ACC and OFC) may be able to reduce the amplitude of the phasic trail of neural activity in Ia. Verhagen et al. but varied between subjects (Schoenfeld et al. The only modularity found thus far in the orolfactory systems is that of the olfactory bulb with its glomerular structure (Bozza et al. Lamme and Roelfsema (2000) have presented several arguments suggesting recurrent activation in the visual system: dynamic tuning and non-classical receptive fields.. Thus I propose that awareness of intraoral food is related to the concomitant reverberant selfsustained activation of a coalition (in Crick and Koch's terminology) of neuronal subsets in Ia-OFC (affect. 2001). there is no direct evidence for recurrent activation in orolfactory neural structures derived from higher order reciprocal cortical connections. It may well be that the combined OB-aPC-pPC-OFC/Ag/PrC/ErC (see Haberly. 1997) showing sustained activity. in terms of similarity in gustatory tuning of neurons located along recording tracts orthogonal to the cortical surface. It is emphasized that different aspects of visual entities may not become “microconscious” at the same . In a recent review (which included a meta-analysis of 87 imaging studies). in individual electrode tracks made orthogonal to the cortical laminae (e. He proposes the term “microconsciousness. it was indeed found that the functional organization may be along a medial–lateral axis. 2001). neurons with vastly different tuning profiles within a modality have been encountered in the caudolateral OFC (Walker's area 12). 1988). it may be that the essential nodes/neural ensembles as related to vision may be of a different structure than those of the orolfactory systems. In contrast to the OB. V4 for color vision. V4 color coding. given our current hypothesis that OFC would be mainly involved with the affect awareness. we would expect an organization related to reward value. these may consist of cortical modules (each with coherent featural sensitivity. Hence.g. these nodes may consist of ensembles of neurons with similar tuning profiles that do not show clear spatial (e. Indeed.

It will furthermore be of interest to assess to what extent differences in odor versus taste processing as modulated by attention reflects their differential involvement with thalamocortical gating mediated by the thalamic reticular nucleus (Crick. I propose that two overlapping but distinct networks are involved in food object (recognition) awareness and food affective awareness: the agranular insulaperirhinal cortex network and the agranular insula–orbitofrontal cortex–anterior cingulate network. which exists in parallel with Craig's non-oral homeostatic interoceptive system. Amygdala activation can be elicited by emotionally salient stimuli without awareness (Whalen et al. even though under specific laboratory conditions they may become separable. PPC and cingulate gyrus. finding that processes are dissociable does not imply they are typically dissociated). Neurodynamically.. 2003). 1). which have been suggested to be involved in exogenous attentional functions (Corbetta and Shulman.and item-specific level (Chun and Marois.. 2003). as have others (Pessoa et al.6. respectively.e.. Attention has been shown to enhance neural responses in lower visual and auditory areas without changing neural tuning (Chun and Marois. leads to a decrease in latency of early components and to an increase in amplitude of late components (Krauel et al. 2002). such activity sets up a self-sustained reentrant/recurrent net standing wave between higher (heteromodal) and lower (unimodal) cortical areas (essential nodes). activated either the parahippocampal place area or the fusiform face area (fusiform gyrus. For example. which was suggested to be due to their quality fusion into a unique new flavor (Ashkenazi and Marks. as well as to the possibility of neural priming in gustation. the amygdala may show interaction with the right temporoparietal junction and inferior and middle temporal gyri. I provide a very brief discussion on covert attention. 1999). and thus that a “neural glue” is required to enable a subject to become aware of all features of stimulus at the same time. 2002). 2004) and citric acid (Marks and Wheeler. temporal and cingulate cortex. as shown in extinction experiments with patients showing unilateral neglect (Gazzaniga et al. 2002). parietal. Attention did not enhance detectability of sucrose or vanillin when they were presented in the same oral aqueous solution.2. there is converging evidence (mainly from the visual neurosciences) that conscious experience is correlated with activity in higher association cortices like frontal. Conceiving of the taste system as part of a homeostatic system explains several observations not integrated before and may be useful in the investigation of the neural correlates of consciousness.. This network of areas overlaps with the one revealed in neuroimaging studies on attention to visual object features (Pessoa et al. Behaviorally. Emotionally salient stimuli can act as exogenous cues for attention (Gazzaniga et al. It remains to be tested whether this also holds for orolfactory food perception.. Attentional priming occurs in the visual areas which are related to the location and features that attention is directed to (Corbetta et al. but that this merging process would be “postconscious” (consciousness at a later stage. this suggests that the amygdala may be critical for the exogenous attentional cuing to these stimuli. Attentional priming has similarly been reported for the olfactory system in a study investigating event-related potentials (ERP). 1999). electrophysiological and imaging studies. I suggest that the modality of taste may be considered one among several modalities that are represented in a unified system encoding input of the oral cavity.. in images where both stimuli were superimposed on each other. I . 2003). 2002). 2002). in a well-controlled fMRI experiment. It has been found that the amygdala plays a major role in the emotional modulation of attention (Anderson and Phelps. There. compared to ignoring it. 1984). 2004). by providing top-down biasing signals modulating activity in the visual cortex (Pessoa et al.B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 283 time as others. 2. Attentional blindness and change blindness paradigms have shown that we only become aware of a fraction of the information that lies within our visual fields (Rensink. 2002). which is called attentional priming (Gazzaniga et al. 3. Based on this synthesis and anatomical. Gitelman et al. attending to either a house or a face. As orolfactory stimuli can be primary reinforcers (Rolls. 2001). Attending to orthonasally presented odor. It has been proposed that this frontal–parietal network is required for explicit awareness of visual events that are neurally processed up to the category. 2002). 1998). 2002). 1998). 1991). Unattended information may be highly processed without awareness thereof. could this be Zeki's “neural glue”?). aversive words are detected more readily and produce smaller attentional blink errors (Chun and Marois.. 2002). arguing for a “late selection” process (Chun and Marois. thought to be the human analogue of macaque IT). For example.. the oral homeostatic interoceptive sensory system (oHIS). Ashkenazi and Marks (2004) reported that attending to retronasally presented vanillin did not improve its detectability. This may have implications for understanding pathological conditions such as body image and eating disorders as well. Future studies should explore the possibility of behavioral and neural differences when attending to orthonasal versus retronasal odorants.. 1998) and requires attention (Pessoa et al. 2002) and experiments on change blindness and attentional blink. Attention For completeness. (1999) have shown.. interestingly. respectively (O'Craven et al. which may be considered a process that selects which high level information may enter the limited capacity processes of consciousness (the “bottleneck”). A problem in this hypothesis is that objects/events (with respect to color of an object and its movement for example) are “bound” together in our conscious experience. and that hence the “microconscious”/“post-consciousness” interpretation has limited ecological use (i. as the olfactory system anatomically lacks such obligatory thalamic mediation (Fig.. Conclusions In summary. including the frontal eye fields. though attention did improve detectability of sucrose (Ashkenazi and Marks. He suggests that the CNS may require methods to align different microconsciousnesses (feature representations) in time. Mesulam 2000 mentions the functionality of the projections of neural epicenters to the striatum to be “synchronizers”. that frontal and parietal cortical areas mediate the internal “spotlight” of visual spatial attention. up to the semantic level.

M.. Effect of endogenous attention on detection of weak gustatory and olfactory flavors. Brain Res. et al. 87–96. 2003b. 3. Sci.T. Nat. Function of the thalamic reticular complex: the searchlight hypothesis. W. as have been employed in vision.. 2000. Rolls and Mikiko Kadohisa for their collaboration with the multimodal electrophysiology.. Crick.. 180–184. A neuronal network model linking subjective reports and objective physiological data during conscious perception. Marcel Dekker. Neurosci. Nat. Nat. G.. Craig. de Araujo.M..L. anterior cingulate.. A review.J. et al.. Neurosci..L. E.. 428–433. Acad... 2003. 2001. 2002.M.. H.L. The role of the human senses in food acceptance. Nat.. REFERENCES Aato. Control of goal-directed and stimulus-driven attention in the brain... Eur.... 841–864. 16–25.T. M. A. New York.. R. Erickson.L. The dark side of visual attention. Marks. et al. Acknowledgments JVV wishes to thank Drs. 41–52. Cavada. Corbetta. Reciprocal functional connections of the olfactory bulbs and other olfactory related areas with the prefrontal cortex. T. 1994..R. I. E. 19 (6).. M. Ferreyra-Moyano.T.. Phys. Trends Neurosci... may be valuable means for such research.g. J. Nat. 2004. 2002.. 2001... Nat. Opin. Behav. Gen.D. 239–241..R. 2003.). Neurosci. M.. Rolls. Craig. A.E. Shulman. 19. 2003a. Bull. Barbara K. smell. The anatomical connections of the macaque monkey orbitofrontal cortex. Curr. 66 (4).. A. Linster. 303–307. J. 81. A new view of pain as a homeostatic emotion. et al.. Putnam. Wiens.. Neurosci. 1996. Rev. 184–189. R.. R. Neuroscience 64. 1975. Gaffan. J.J. 4586–4590. 2003. M. Christoff. S. 2004. Contreras. 8520–8525. R. 1984.. Trends Cogn.. Human feelings: why are some more aware than others? Trends Cogn. C. and taste of food in the cephalic phase of gastric acid secretion in humans.. Neurosci.).. Richardson.. L. Cereb.P. Edmund T.P... Dissociated effects of perirhinal cortex ablation.K. A. The comments and discussion by Dr.. R. 1987. et al. How do you feel? Interoception: the sense of the physiological condition of the body. H. L. Rolls. 211–218. New York. Proc. Food Choice. M.. 26 (6).K.. Astic. Feldman. 1994. Temporal binding and the neural correlates of sensory consciousness.). 100 (14). 2000. NeuroReport 10 (3). 2000..L. Psychophysical measurement of human olfactory function. A. Neurosci. I suggest that masking tasks and perhaps bistable percepts. Brain Res. D. I.. A. J. Neuroanatomical basis for first. 9–21. C.. C. McGann. Natl..and second-order representations of bodily states. Percept. Critchley. 3 (2). F. Laing.. Chun. T. 6 (2). S.D. Sci. Crick. Cardello. Buck. 3. The function of various brain areas (especially the perirhinal cortex. In: Doty. 801–812. The representation of umami taste in the human brain. Chapter 1. Thermosensory activation of insular cortex. 2001. 2003. Di Lorenzo. Miezin. 1991. 207–212. 119–126. H. J.. S. 313–319.. 4 (2).D. A.. McCaughey. Information coding in the vertebrate olfactory system.. Rev. F. 2383–2402. Ogawa. 220–242. e. C.. Chen. 18. Engel. De Araujo. Nature 411. 305–309. Natl. Dissociated neural representations of intensity and valence in human olfaction.K. MacFie. Damasio.. L.V. Phys. 100 (9).D. 655–666.A. JVV is supported by NIH grant R03 DC008197-01 to JVV. 1996. Behav. 1999. the neural correlates of attention to and consciousness of food flavor or its components have thus far been unexplored. Anderson. 196–202. D. Central olfactory pathways.A. G. Anderson. Sci. F. (Eds. Baylis.. Francis. S. Nature 413. Physiol. Neurosci.G. T. Sergent. Phelps. 2000. Rev. H. R. (Ed. A framework for consciousness. H.. K.L. Company. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Neurosci. via differential activation of gradients across the Ia and OFC. 6... (Ed. et al. A.284 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 suggest that the essential nodes involve different neural sets than those of vision. Annu. for example by studying the perception of flavors in patients or monkeys with welldefined lesions in these areas and other standard techniques. et al. Scott. 442. Nat. 11 (8). L. London. insula and OFC) in flavor perception needs further exploration.. 596–608. Phys. including odorant mixture assessment. et al. et al. 189–195. Neuron 42... Acceptance and Consumption.. 2003. Craig. 2003. The overall conscious experience of food identity and affect would involve the synchronous reciprocal activation among these areas. Cinellar. Barry Green are gratefully acknowledged. New York. 1994. and the representation of the pleasantness of flavour. Rev. Giza. color.. 201–215. 5520–5524.D. Psychophys. 2001. Stuart A. 66 (6). 517–544.. 2000. Koch. 2002. Blackie Academic... Proc. Proc. Kringelbach.. Gastroenterology 90. Critchley. M. in the human brain. 781–810.. The evolution of neural coding ideas in the chemical senses. In vivo imaging of neuronal activity by targeted expression of a genetically encoded probe in the mouse.T.T. A. 1988.E. Firestein. E..J. Thomas R. Corbetta. A. Lundy Jr.. Cleland. Neurosci. 1986. Behav. P. Acad.. 453–459. Dehaene. The neural code for taste in the brain stem: response profiles. The representation of pleasant touch in the brain and its relationship with taste and olfactory areas. 69. et al. fornix transection and amygdalectomy: evidence for multiple .M. Sci. et al.. In: Meiselman. Neurophysiol. Response properties of macaque chorda tympani fibers. H. Descartes' Error.. 90. 2059–2068. Cattarelli. Mathias. Neuroscience 56 (4). Taste-olfactory convergence. Handbook of Olfaction and Gustation. 184–190. R. Neural systems supporting interoceptive awareness. Singer. 3–13. Metabolic mapping of 2DG uptake in the rat piriform cortex using computerized image processing. 8 (6). H. Edelman. 2004. Neurosci. Cortex 10 (3). and speed: functional anatomy by positron emission tomography.H. Ashkenazi... Unfortunately. 1993. Rolls. Role of thought.. Doty. Craig. 69. In: Doty. Neurobiol.L. E. 651–662.. 5 (1). sight.F. Acad. 7 (2). Naturalizing consciousness: a theoretical framework.. Afferent connections of the orbitofrontal cortex taste area of the primate. Selective and divided attention during visual discriminations of shape. et al.. Natl. Sci. K. Gustatory neuron types in the periphery: a functional perspective. Bozza. et al. Handbook of Olfaction and Gustation. 12. Marois.D. C. Barbas. Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey. C. et al. 2004. M. How the olfactory system makes sense of scents.T. 69. A. et al.E. Marcel Dekker. 2003.

.. 2003. 411–422. et al.A. Ogawa.. 1997. 1998. Principles of Behavioral and Cognitive Neurology. Lesions of the primate rhinal cortex cause deficits in flavour-visual associative memory.. L. et al. (Ed. Liver Physiol. Physiol. Llinas.. 207–221. M. and taste of foods...J. B. Psychol. Perceptual-mnemonic function of the perirhinal cortex. Nobre. Ribary. Kringelbach. T.B. Neurobiol. Pessoa.B. 341–372. 99–105. H. G.. Gaffan.. Brain Res. et al.L.R. 1984.. et al.J. 61 (1). Brain Res.. memory.T. 1989. Am. 2001. Chem. Neural substrates of crossmodal association memory in monkeys: the amygdala versus the anterior rhinal cortex. Marks. Grossberg.K. Handbook of Olfaction and Gustation. Curr. V. Moon. Am. grittiness. I. Ronnett.. Neurobiol. Kadohisa. Baylis..G. The central gustatory system in humans.R. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. 45–60. Physiol.. J. 415–420. Lateral hypothalamic modulation of oral sensory afferent activity in nucleus tractus solitarius neurons of rats. Inoue. Springer-Verlag. 1996. B. K.R.. Neuroscience 132. E. 2000. E. The thalamocortical dialogue in health and disease.A.. 2003. Norgren. (Ed. J. 23 (11). New York. 289–298. Neurosci. olfactory.. Curr. T.. 1998. Nicolelis. Technol. R. Lamme. Heimer. Molecular physiology of gustatory transduction. Comp. 2004. Neurosci. L. Norgren..J.. T. Prefer.. J. 99 (3). From sensation to perception. Physiol. B.. Physiol. Maller. 33–48. E. 95–106. 188–193. The Brain and Emotion. N. Haberly. Prescott. Rolls. Attention and the detectibility of weak taste stimuli..F.T.. L. Parker. et al.). R..). Chem. O'Doherty. Norgren. et al..L. Chem. L. 1315–1321. Rev. Ogawa.. et al. 329–341. 54 (1). 2001. Oxford University Press. 1999. et al. W..W.L. Areas of the orbitofrontal cortex and amygdala activated by pleasant and unpleasant taste.T.. L. Opin. Murray.. M. Goulet.L.. Green. 223–240. 10.T. Flavour as a psychological construct: implications for perceiving and measuring the sensory qualities of foods... Selective attention and orienting.M. 2000. Neurophysiol. R.. E. 457.C. Some aspects of chemo-reception in human nutrition. 2002. 1967. H. 379 (2). Am. (Ed. Contreras. 1995. 11..B. Kadohisa. 3 (4). Multiple sensitivity of chorda typani fibres of the rat and hamster to gustatory and thermal stimuli. The Human Brain and Spinal Cord. R.. fat texture. Sato. R.. New York. Role of perirhinal cortex in object perception. Trends Food Sci. 2001.). Chem. The attentive brain. Ivry.-M. 1995. Senses 22 (3). 1983. Neurol. J. 1994. et al. 23 (10). Norton and Company. Molecular neurobiology of olfactory transduction. H. Rev. 2001. (Lond.T. Proc..A. 115 (2). 2004. L. Bussey. R. 142–151. Neurosci. 1994. Senses 23 (1). In: Doty.. 93. A large-scale distributed network for covert spatial attention.-M. Opin.J. 2003. Senses 23 (4).V..... Neural activity of chorda tympani mechanosensitive fibers during licking behavior in rats.. et al. J. Am.F. M. Shimizu. Kreiman. 1999. Neurobiol.. Rolls. D. Parallel-distributed processing in olfactory cortex: new insight from morphological and physiological analysis of neuronal circuitry. E. Attentional modulation of central odor processing. Rolls. Neuroscience 126. Rolls.T. New York. et al. N.. et al. 76 (3). C. Behav. Sci. 2002. Soc. 423–432. Acad.C. E. E. Academic. 99. Hayama. Odor-evoked activity is spatially distributed in piriform cortex. 261–270. The distinct modes of vision offered by feedforward and recurrent processing.. Rev. E. Oxford. P.. Thermal sensitivity of neurons in the rostral part of the rat solitary nucleus. Physiological properties and cytoarchitecture. Trends Neurosci. and visual .. 1984. 10. Sci. 2000. The primate amygdala: neuronal representations of the viscosity. J. 4 (5). 1988. 2004. Soc. In: Doty. Marcel Dekker. Mountcastle. Sensory systems.. E. Brain Res. B. et al. 361–367. Rolls. 144. D. 349–356. Rees.. 3. et al. et al... pp.. 1998. 438–449. 3990–3998.A. Neurosci. Neural correlates of consciousness in humans. Senses 26.E. Prog. R. Trends Neurosci. N. Handbook of Olfaction and Gustation. Consciousness and the brain. 584–587. 2004.E.. Food for thought: hedonic experience beyond homeostasis in the human brain. Brain Res. 1996. Laurent.).Y. 1997.. Murray. 83. Central neural mechanisms of taste. E.. Neuroscience 127 (1). 1999.E. J. Downing. 85. Kosar. 234–237. R. 321–331. Oxford University Press.: Gasterointest. Gril.B RA I N RE SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 285 memory systems in the primate temporal lobe.A. Oxford. Matsuo.. T... R. Orbitofrontal cortex: neuronal representation of oral temperature and capsaicin in addition to taste and texture. J.M. The representation of pleasant and aversive taste in the human brain. Otolaryngol. R.. J. Marcel Dekker. Sci. 1999.T. M.. Margolskee. Perceived irritation during ingestion of capsaicin or piperine: comparison of trigeminal and non-trigeminal areas. Brain Res. Nat.. 2003. 929.A. J. V.. D. Pritchard. 2001. Logothetis. Gilbertson. 244–299. 3. 2002.R. Mesulam. Brain 122. O'Craven. M. Natl. 1996. U.M. 1986. Pessoa. S. Johns Hopkins University. Hamilton. Neural coding of gustatory information in the thalamus of Macaca mulatta.. pp. 631–641.. 72. 278 (1).F. G. Behav. 1988. The Human Nervous System. Acad. M.. 1013–1052. 807–819.B. In: Paxinos. Rolls. M.. Brain 120 (4). R. The Chemical Senses and Nutrition. T. Rolls. 4 (4). K.. Matsuo. 245–277. 1087–1128. Pangborn. 551–576. et al. 19–29. 701–722. R. Bethesda.. Neurosci. S.. Nature 401. Behav.. Neuroimaging studies of attention: from modulation of sensory processing to top-down control. Gustatory cortex in the rat: I. Rentmeister-Bryant. Illig. Annu. et al. G. (Ed. M. E. 271–284. Rolls. Sci. New York. Katz. 719–765. 2002. 2005. R. 257–266. 1968. 1093–1106. Cognitive Neuroscience.. K. A. Gustatory.. MD. L. Baltimore.. Consciousness absent and present: a neurophysiological exploration..... Trends Cogn. 1–14. Roelfsema.. M... 1993.. P. Ann. Brain Res. 166–175.A. 25. Kastner. Mesulam. 1998. O'Doherty. Food Qual... Exp. The columnar organization of the neocortex. The gustatory system in mammals. G. fMRI evidence for objects as the units of attentional selection. Pause.. J. Dynamical representation of odors by oscillating and evolving neural assemblies. Green.. Richmond. R.. 19 (11). M.. 7. Hudspeth. Krauel.A... G6–G9. Chemesthesis: pungency as a component of flavor. McKenna. Gitelman. Neural processing of emotional faces requires attention. Neurophysiol. 11458–11463. There is more to taste than meets the tongue.T. E. Wheeler. In: Kare. 1201–1207. Brain 121. Change detection.. Taste reception. Nutrient tasting and signaling mechanisms in the gut: IV.. 454 (1–2).L. M. M. and associations. 65–70. O.S.. Kringelbach.. Prog. Rensink... pp. Physiol. 1999. 2000. B. Lindemann.. Taste prestimulation increases the chorda tympani nerve response to menthol. H... 689 (2).).J...B. G. 1999. et al. S.) 199 (1). Lundy Jr. R. E. A.. 53. In: Darian-Smith.B.. Murray. Handbook of Physiology—The Nervous System.. Haberly.G. (Eds. 489–496. Gazzaniga.

Schoenfeld. L. J. Mass..J.. B. 2003..T. Marcel Dekker. E. Trends Food Sci. 7–14. D. The responsiveness of neurones in the frontal opercular gustatory cortex of the macaque monkey is independent of hunger.T. 442–472. T. 2000. Technol. Schultz. Gustatory neural coding. Scott. 2003.. Rev. Behav.P. Verhagen. S.. Taste responses of cortical neurons in freely ingesting rats. Rolls.V.L. Whalen. The primate insular/opercular taste cortex: neuronal representations of the viscosity. J.T. J. J.. 67. J. et al.J. Malkova. (Ed...L. In: Doty..).M.. T.V.).. Neural coding of gustatory information. E... John... Verhagen. Thieme Medical Publishers. Small. A. 1–39.. 18. 1263–1289. Taste in the monkey cortex.. T.. NeuroReport 10 (1).. 655–664. Functional neuroimaging of human olfaction. Neurosci..C. et al. T. The Cognitive Neurosciences.J. 1999. 1989.H. Small.R. 874–885.. 293–317.K. et al. Sienkiewicz. 1996. St. 32. Zatorre.R. L. R. R. 271–283.. Neurosci. Neuron 40. T.J.V. 24.N.. New York. Rev. 281–292.. J. pp. et al. Verhagen. N. Wicker... et al.. New York.. Engelen.K... Brain 124. Brain Res. K.L. Neurobiology 3 (3–4). C. Deco. G. Human cortical gustatory areas: a review of functional neuroimaging data. 455–461. 165–181. Marcel Dekker. 147–159... Smell and Taste in Health and Disease. Yan.. 2001. grittiness.. 1983. J. E. Pardo. (Ed. Neuer. T. 2000.R.. 395–407.. 1020–1025. Zald. 77–85. (Ed.. T.. R. J. H. 1995... 1992. 2003. pp. Rolls. E. E. Concurrent processing in the primate visual cortex. New York.A.. 1–12. A. Handbook of Olfaction and Gustation. 57–86. Tovee.. 2004. T. Neurons in the primate orbitofrontal cortex respond to fat texture independently of viscosity.. 2001... Biobehav. Chap. De Yoe. 1989. Physiol. Oscillatory activity is not evident in the primate temporal visual cortex with static stimuli. 2000..... Nutritional Triggers for Health and Disease.. J. S. Sewards. Sobel.R. et al.J.. Curr. S. 2002.. 143–149. 1514–1525. T. B. Genetic tracing reveals a stereotyped sensory map in the olfactory cortex. Imaging of brain activation by odorants in humans.. 1992. et al. Co-Planar Stereotaxic Atlas of the Human Brain. Smith. M. Rolls. W. Hunger modulates the responses to gustatory stimuli of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. Z. Yamamoto. Verhagen. Prog. N. Giza.T. R. 27. 272–284. Grabauskiene. et al. T. 613–650. Yuyama. 265–275. P. Nature 414. 53–60. New York. Karger. Scott. 369–372.R. Satinoff. D.. Rolls. Savic. Psychophysiol. et al.R.. M.. Nutrition 16. E. Localization and globalization in conscious vision. et al. Handbook of Olfaction and Gustation.. D. A reevaluation of the concept of the homeostatic organization of temperature regulation. Satiety does not affect gustatory activity in the nucleus of the solitary tract of the alert monkey. Neurophysiol.. 62. New York. G. Matsuo.. Behav. 90. M. Verhagen.D. 173–179. 1991. 1986. Basel. et al. T. Cortical neurons responding to tactile. Van Essen.. D. 90. Raven Press. Neurosci.. Long-term recording from the chorda tympani nerve in rats. et al. M.). Brain Res. P. Scott. pp. thermal and taste stimulations of the rat's tongue. T. 383–400. R. New York... girttiness and capsaicin. 2000. Dual separate pathways for sensory and hedonic aspects of taste. J. Neurobiol... 448–452. T. Scott.V. D. Int. Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge.A. Consciousness. Yaxley. (Ed. J. In: Gazzaniga. et al. 36 (2).. et al. 221.286 B RA I N R E SE A R CH RE V I EW S 53 ( 20 0 7 ) 2 7 1–2 8 6 convergence within the primate orbitofrontal cortex. 7. 1985. Functional neuroimaging of the olfactory system in humans. 2002. 30 (5). Yamamoto. Small. Functional magnetic resonance tomography correlates of taste perception in the human primary taste cortex.R. 61 (6). Shimatani. Handbook of Olfaction and Gustation.R. J... S. R. 1981.M. 1988. 679–705. NeuroReport 15 (1).. 2006. 2001. Wilson.R. Brain mechanisms of satiety and taste in macaques.. 1999. 1720–1733.. Keysers. Computational Neuroscience of Vision.F. Teitelbaum.. J. 65–76. Rolls. 3711–3724... et al. 2000. 1988.M.. Oxford University Press. (Ed. 2004. 85–93. Taste quality and neural coding: implications from psychophysics and neurophysiology. Cortical spatial aspects of optical intrinsic signals in response to sucrose and NaCl stimuli. 67 (4). In: Satinoff. 2003.V. Changes in brain activity related to eating chocolate from pleasure to aversion.. 2002. Handbook of Olfaction and Gustation. Giza.. Behav. Neurophys. Marcel Dekker. Verhagen. Smith. Mark.. Scott. Coding of Taste Quality. Zeman. D.V. Tremblay. MIT. 1995. Tournoux. 112 (4). Curr. Neural cell types and taste quality coding. 2001.). St. D. M. et al. 347 (1). 701–711. J.V. Neurophys. Rolls. Cortical association areas in the gustatory system. Dekker.A.V. Cortex 10 (3). Neurosci. In: Doty. Scott. Sugai. Sewards. Smith.V. 1999. D. C. E.A. Behav. Dissociation of neural representation of intensity and affective valuation in human gustation. 489–511.R. J. Zou. Rev. Johnson. Neuron 14. J. Z. Biobehav. Behav. (Ed. E. Yoshimura. pp. P.. .T.) 397. J. 1998. 69. Phys. 92. (Lond. 1685–1699.. Taste as a factor in the management of nutrition. T. Inc. Neurobiol. Neurophysiol. Rhinal cortex ablations fail to disrupt reinforcer devaluation effects in rhesus monkeys (Macaca mulatta).R. Scott. J. John. Zald. Schiffman. J.T. In: Doty.. E. G. Teff. C.M. 17–20. 5437–5452.V. T. 1. Rolls. Neurosci.T.. S..V. 347–353.. 14 (9). Neurosci. Brain Res. et al.. In: Doty. Rolls.. B. 2000. Horowitz... 2004. Annu. Zeki.J. In: Getchell. et al.L. Eur.. Opin. Cereb. 1998. Reward processing in primate orbitofrontal cortex and basal ganglia. NeuroReport 3 (4). et al. Rauch. et al.R. Neurophysiol. D. Scott.. 9 (4). 2003a.L. Oxford. 12. 6.V. Issues of gustatory neural coding: where they stand today.. 1244–1258. 69. 2004. Sensory physiology of central olfactory pathways. Behav. 69. Physiol. Neurosci. Sewards.A.). E. et al.). The neurocognitive bases of human multimodal food perception: sensory integration. S. 2001. 25. Handbook of Behavioral Neurobiology. 76 (1). Physiological effects of flavour perception.. 2003.. fat texture. L. L. Responses to taste stimulation in the ventroposteromedial nucleus of the thalamus in rats. Kadohisa. E. temperature and taste of foods. Physiol.. Neuroscience 127. New York. 411–418. 427–435. Neurobiol.. Plata-Salaman. Phys.... J.. et al. Opin. Y. Scott.S.. 202–206. Thornton. et al. 2003. (Ed. Brain 124. Representations of the texture of food in the primate orbitofrontal cortex: neurons responding to viscosity. (Eds. Scott. 2003... 89.H.V. 2003b.. I. S. Physiol. Gregory. In: Simopoulos. Feeding and taste. T. Plenum Press..).. Taste: the neural basis of body wisdom.... M. D.). Sullivan. R. B.T. Talairach. Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Plata-Salaman. Cambridge.. Bull. Central taste anatomy and neurophysiology.L..

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