Elsevier

NeuroImage

Volume 31, Issue 2, June 2006, Pages 796-806
NeuroImage

Prefrontal activity during taste encoding: An fNIRS study

https://doi.org/10.1016/j.neuroimage.2005.12.021Get rights and content

Abstract

To elucidate the function of the lateral prefrontal cortex (LPFC) in taste encoding, it is worth applying to taste, the psychological paradigms of intentional memorization that have been used with other extensively studied senses, and thus updating current models for LPFC functions to include a taste modality. Using multichannel functional near-infrared spectroscopy (fNIRS), we examined the LPFC's of healthy volunteers (N = 18) during the intentional memorization of a basic taste. In order to minimize the confounding effects of verbal processes that are known to employ the left LPFC, we used quaternary taste mixtures that were difficult to verbalize, and confined analysis to those who did not use a verbal strategy during memorization (N = 10). In order to examine the results in association with data in the literature, the location of activity was probabilistically estimated and anatomically labeled in the Montreal Neurological Institute (MNI) standard brain space. By contrasting the cortical activation under encoding conditions with that under control conditions without memory requirement, we found activation in the bilateral ventro-LPFC and the right posterior portion of the LPFC. The activation pattern was consistent with previous studies on the encoding of nonverbal materials using other senses. This suggests that models for LPFC functions that derive from previous studies can be generalized to intentional encoding processes of taste information, at least at a macro-structural level. The current study also demonstrates that, by using fNIRS, LPFC functions on taste can be examined with experimental paradigms relevant to those used for other senses.

Introduction

While the importance of the lateral prefrontal cortex (LPFC) in taste processing is gradually drawing attention (Kringelbach et al., 2004), LPFC functions associated with taste are still largely unexplored. Current models for LPFC functions are derived mostly from extensive studies with visual and auditory modalities. As amodal role for the LPFC is widely assumed, these models may be applicable to taste modality. However, LPFC organization has proven to be complex, and the existence of sensory-specific neural circuits is also suggested (Ruchkin et al., 1997, Crottaz-Herbette et al., 2004, Rama and Courtney, 2005). It is therefore worthwhile to examine LPFC functions with taste to update the current models to include a taste modality.

In this study, we focused on the LPFC role in the intentional memorization of tastes. In the cognitive neuropsychology of memory, this process is categorized as intentional episodic memory encoding, or intentional encoding of personally experienced past events (Tulving, 1983). A wealth of neuroimaging studies have examined the neural basis for episodic memory encoding for visually presented stimuli and have shown LPFC involvement. The LPFC activation was also found in studies using auditory (Fletcher et al., 1995, Frey et al., 2004) and somatosensory stimuli (Stoeckel et al., 2003). According to the current memory model based on these neuroimaging studies, as well as electrophysiological and neuropsychological memory studies, the LPFC plays a crucial role in effortful memory formation: it sorts, searches, recombines, selects, and reintegrates information, which is stored at the modality-specific areas of the relevant information in the posterior cortices (Mesulam, 1998). In this model, the limbic system is also thought to play an integral part by providing a directory that guides the binding of the modality and category-specific fragments of individual events to form coherent multimodal experiences.

Regarding gustatory memory, animal studies have indicated the involvement of the gustatory cortex and limbic regions in taste-memory formation, and this is in line with the above model (Bahar et al., 2004, Burke et al., 2005). With humans, several studies have shown the involvement of the insular, the limbic system, and the LPFC in taste imagery, which is assumed to involve a memory retrieval process (Levy et al., 1999, Kobayashi et al., 2004). However, to our knowledge, there has been no attempt to examine the LPFC's role in intentional taste memory formation. It is interesting to note that Dade et al. (2002) examined cortical activity related to olfactory encoding using positron emission tomography (PET), and did not find activation in LPFC areas, but only in the premotor areas (Brodmann area 4, 6, and 8). Anatomically, both gustation and olfaction are different from other senses. Primary representation of vision, audition, and somatosensation occurs in the unimodal neocortex. On the other hand, early representation of taste and smell arises in heteromodal regions in the paralimbic and orbitofrontal regions (Zatorre et al., 1992, Kobayakawa et al., 1996), which are known to be closely associated with memory (Mesulam, 1998, Frey and Petrides, 2000, Frey and Petrides, 2002). As the LPFC is assumed to fulfill its role in memory formation together with sensory-specific and limbic regions, its role in regard to taste and olfactory sensory information, given their anatomical traits, may differ, and this may be reflected in its activation pattern. Therefore, our first question is whether the encoding of taste sensations recruits those LPFC regions demonstrated to be involved in encoding of visual, auditory, and somatosensory sensations.

The second question is the laterality. In memory studies, the encoding of verbal materials almost always exhibited left-lateralized LPFC activations, while encoding conditions involving nonverbal materials yielded bilateral and right-lateralized activation (reviewed by Cabeza and Nyberg, 2000). Therefore, the degree of verbalization of the material to be encoded is hypothesized to determine the laterality. As taste sensation has not been examined in the context of memory encoding, we are interested in whether a hemispheric asymmetry can be seen in taste encoding as has been found to be the case in studies resulting in the above hypothesis.

We set up an encoding task that minimizes verbal processes that are known to employ the left LPFC. Our hope was that, in this manner, the LPFC functions related to the encoding of taste sensation could be isolated. For this, we prepared taste solutions consisting of four of the five basic tastes (sweet, sour, salty, and umami) in slightly different concentrations. The resultant complex taste solutions were difficult to describe adequately with verbal labels used to aid recognition, restricting the effectiveness of verbal labeling strategies. Moreover, based on a post hoc questionnaire, we excluded data from those who employed verbal codes for memorization.

We used functional near-infrared spectroscopy (fNIRS), an optical method that noninvasively measure lateral cortical hemodynamics (Strangman et al., 2002a, Hoshi, 2003, Obrig and Villringer, 2003), to monitor LPFC activity. Compared to other neuroimaging methods, fNIRS is relatively forgiving of body movement and less restrictive, allowing brain functions to be examined under relatively natural tasting conditions. This is advantageous in studying the cognitive processes of taste, as difficulty in tasting in restricted or unnatural body positions may pose an additional cognitive load on the subjects. However, as fNIRS data are obtained on the head surface without any structural information of the brain, it can be difficult to identify the exact brain region of the activated foci. To cope with this, we implemented a method we developed in previous studies that probabilistically registers fNIRS data to the standard Montreal Neurological Institute (MNI) space, and reported their spatial information in a manner compatible with other neuroimaging studies (Okamoto et al., 2004b, Jurcak et al., 2005, Okamoto and Dan, 2005, Singh et al., 2005). Moreover, we functionally distinguish oral sensorimotor areas from the neighboring ventrolateral prefrontal cortex (VLPFC), which has been related to encoding tasks in previous studies, by asking subjects to conduct a tongue movement task.

In this way, we aimed to examine whether LPFC regions similar to those which have been identified in other intensively researched sensory systems are involved in the intentional memory formation of gustatory modality with a minimal use of verbal strategy.

Section snippets

Subjects

Out of the 18 right-handed healthy volunteers who participated in this study, we analyzed data from 10 subjects (four males and six females, aged 25 to 44 years) who did not use verbal codes for memorization of the taste samples. Subjects who used verbal codes during any of the trials in encoding session were identified by use of a post hoc questionnaire (five subjects). Three subjects, who exhibited considerable fNIRS signal changes of ΔtotalHb > 0.1 mM–mm between two consecutive time points

Results

In order to effectively compare our fNIRS results on taste encoding with results from other neuroimaging studies, most of which are presented in common stereotaxic space, we probabilistically estimated the coordinate values and corresponding anatomical regions in MNI space (Fig. 3A, Table 2). The channels covered the inferior frontal gyrus (IFG), the middle frontal gyrus (MFG), and the pre- and postcentral gyri. Among them, the channels on the postcentral gyri exhibited significant activation

Discussion

The primary question addressed in the present study is whether LPFC regions similar to those which have been identified in more heavily researched sensory systems are involved in intentional memory encoding of gustatory modality.

Previous studies on intentional episodic memory encoding usually found activation in the LPFC, although activation foci ranged widely across studies. We have plotted activation foci from relevant studies, on MNI space, together with our results in Fig. 3C. As Fig. 3C

Acknowledgments

We thank the subjects who participated in this study. We are grateful to Ms. Archana Singh, Dr. Fumiyo Hayakawa, and Dr. Yuji Wada for their helpful advice. We thank Mr. Valer Jurcak for preparation of figures, Ms. Akiko Oishi and Ms. Yumiko Shiga for preparation of the manuscript and data, and Ms. Melissa Nuytten for examination of the manuscript. This work is supported by the Program for Promotion of Basic Research Activities for Innovative Bioscience (PROBRAIN), and the Industrial Technology

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