Spatio-temporal correlates of taste processing in the human primary gustatory cortex
Introduction
Brain regions receiving direct sensory information from the thalamus are referred to as primary sensory areas. These primary areas are well established for somato-sensation, vision, or audition. However, for the sense of taste the site of the primary gustatory cortex (PGC) in humans is still being debated. Studies performed in non-human primates suggested a divided primary representation in the anterior primary somatosensory cortex (BA 3b) and in the anterior part of the insula and overlaying operculum (Pritchard et al., 1986).
Studies in humans based on cerebral lesions report gustatory disturbances typically when the insula is damaged in the rostral (Motta, 1959, Pritchard et al., 1999, Cereda et al., 2002) left posterior (Cereda et al., 2002) or more generally in different regions of the insular cortex (Henkin et al., 1977, Pritchard et al., 1999), but also for parietal and frontal operculum lesions (Hausser-Hauw and Bancaud, 1987).
Neuroimaging studies on gustatory function in humans using functional magnetic resonance imaging (fMRI), positron emission tomography (PET), magneto-encephalography (MEG) or electroencephalography (EEG) report activations in several locations in the insular cortex and overlying operculum. (Small et al., 1997, Frey and Petrides, 1999, de Araujo et al., 2003a, de Araujo et al., 2003b, Schoenfeld et al., 2004, Ogawa et al., 2005, Veldhuizen et al., 2007, Seo et al., 2011, Iannilli et al., 2012. Nevertheless, meta-analyses of those studies failed to precisely localize or identify sub-regions within the insula and operculum in order to provide a clear definition of the primary taste cortex (Small, 2010, Veldhuizen et al., 2011). Several reasons can account for this controversy: heterogeneity in function and structures of insular cortex, differences in neuroimaging techniques as well as difficulty to control the precise delivery of taste stimuli.
The insula cortex in humans is a multimodal integration region. It is subdivided by three cytoarchitectonical sub-structures: the anterior agranular area, the posterior granular area, and the transitional dysgranular zone, which are also functionally diverse. A wide range of exogenous as well as endogenous conditions seem to produce activation in these regions. Interoception, pain, or emphatic feeling, but also awareness of body movement and emotions as well as speech, have been correlated with activations in the insular cortex (Craig, 2009). Thermal, (Craig et al., 2000, Guest et al., 2007), somatosensory (Iannilli et al., 2008), olfactory (Gottfried, 2010) or multisensory aspects of taste encoding (de Araujo et al., 2003c) also seem to be processed inside the insular cortex together with the main perceptual categories of taste (Mizoguchi et al., 2002, de Araujo et al., 2003a, de Araujo et al., 2003b, Schoenfeld et al., 2004, Ogawa et al., 2005, Iannilli et al., 2012. On the other hand, when activity of single neurons was recorded in the primary taste cortex of 11 alert macaques only 6% of all neurons responded exclusively to taste stimuli(Scott and Plata-Salaman, 1999) suggesting a rather sparse distribution of taste cells in this region. In addition, considering that several oral sensory experiences co-occur with taste sensations, the processing of which is also co-localized in the insular cortex it is not surprising that the location of the primary taste cortex is still vaguely defined.
The employed neuroimaging modality is a major factor when it comes to the localization of the primary taste cortex. fMRI and PET detect hemodynamic changes in the brain. Typically they have a good spatial resolution of 1–3 mm compared to the accuracy of source localization achieved with multichannel-EEG or MEG. On the other hand, the temporal resolution of PET and fMRI is limited by the relatively slow metabolic changes that occur typically in the range of a few seconds. In the specific situation of taste, experiments are often designed in a so-called “block design”, that is fMRI and PET show brain activity correlated with the specific task, mediated over space (1–3 mm) and time (20–30 s) compared to a control state where the taste stimulus is absent. The definition of the control state in experiments on the neural correlates of taste is crucial: it must consist of a condition with tasteless solution which is not different in other physicochemical characteristics from a taste stimulus, e.g. temperature and texture. It has been demonstrated that the use of water is problematic as it seems to induce taste like activities in various insular areas (de Araujo et al., 2003a, de Araujo et al., 2003b) and when used as a control condition it can mask brain areas involved in taste perception. A challenge is also to handle the application of liquid solutions in the scanner environment, as well as movement artifacts due to the rinsing and swallowing. One possibility is to instruct subjects visually to keep small boluses (1 ml) in the mouth for a time, then swallow it and then to rinse with a rinsing solution (Iannilli et al., 2012).
Aim of this work was to investigate the location of the PGC using source analysis of high density – channel MEG and EEG recordings – systems which allow signal analysis with an excellent temporal solution other than what is possible with fMRI or PET.
Section snippets
Subjects
Fourteen healthy subjects (seven female, mean ages ± s.d. = 26 ± 3 years) participated as volunteers in the study. All gave informed consent. The local ethics committee approved the study. Subjects received moderate remuneration for participation.
Stimuli and taste stimulator
Stimuli were delivered by means of a computer-controlled taste pulse system to which we will refer along the manuscript as “gustometer” (Gu002/GM05, Burghart, Wedel, Germany), Fig. 1. The gustometer delivers small volumes of solutions in a pulsed fashion
Psychophysical rating
The two stimuli were perceived at the same intensity level (mean-salt ± s.e. = 6 ± 1; intensity-mean-sweet ± s.e. = 7 ± 1; T-test = 0.90; p = 0.38); in addition, there was no significant difference in terms of the pleasantness of the two stimuli (sweet: mean ± s.e. = 0.7 ± 1.0; salt: mean ± s.e. = −0.4 ± 0.8; t-test = 1.90; p = 0.07).
Although the experiment was carried out using two stimulus conditions, the results focus only on the salt condition, in fact the signal to noise ratio (SNR) in the sweet conditions was not good
Discussion
The focus of this work was to look for the primary taste cortex in humans. To this end we used a state-of-the-art gustometer, which compared to other taste stimuli devices like the gustometer proposed by Kobayakawa and colleagues (Onoda et al., 2005) or the electrogustometer (Ohla et al., 2009) combine the precise control of the stimulus onset, temperature and reduction of mechano-sensory stimulation to a wide set of taste stimuli combination. The same device has been demonstrated to elicit
Conclusion
In conclusion the main result of the present study was a position shift from an early response located in the middle insula, and a later response, located in a more posterior part. Together with previous neuroimaging results, our findings suggest the anterior/middle insula as a location for the primary taste response.
Acknowledgment
We are thankful to Benno Schuster for his help during recording of the data.
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