Time for Taste-A Review of the Early Cerebral Processing of Gustatory Perception

Time for Taste-A Review of the Early Cerebral Processing of Gustatory Perception

Abstract The first successfully recorded event-related potential for taste, one of our basic senses, was published nearly half a century ago. Despite this large time span, surprisingly little is known about the early neural processing of taste perception. Here, we are providing a comprehensive and critical overview of over four decades of research, with a focus on the temporal dimension of cerebral taste processing in healthy humans. For this purpose, we review studies using techniques that permit a high temporal resolution, namely, electroencephalography and magnetoencephalography, ERP, and event-related magnetic fields. Our current knowledge of taste ERP is interpreted in the context of our understanding of other, nonchemical senses. Gaps in the existing literature are identified and discussed. Finally, we suggest directions for future investigations using gustatory ERP/ERF.

Cortical Taste Processing

Compared to the other sensory systems, relatively little is known of how the human brain processes taste. This is surprising, given the central role of gustation in food intake. The sense of taste provides a gateway for energy and nutrient balance and, as such, is instrumental in the selection of foods. Information conveyed via the gustatory system aids in identifying edible and nutritious food sources, enables us to avoid poisonous substances, as well as drives the hedonic evaluation of potential nutrition, which can take place prior to, during, or after ingestion. Therefore, gustation serves a vital function that calls for efficient coupling of perception and behavior in order to allow a fast behavioral response, e.g., spitting out a potentially noxious food. It is for this reason, among others, that the interest in understanding gustatory processing is growing, not only for basic science, but also for clinical applications and the consumer industry.

While some of the aforementioned taste-related processes can be performed at the level of the brain stem, taste afferents project to and activate various regions of the neocortex where the intensity, quality, and reward value of taste are processed. Most of our current understanding of the cortical areas involved in human taste perception has been derived from functional neuroimaging studies using either functional magnetic resonance imaging or positron emission tomography. These studies have shown that liquid oral stimuli activate several subdivisions of the insula, orbitofrontal cortex, and anterior cingulate cortex. According to a recent meta-analysis of all available gustatory functional imaging papers, a significant and widespread probability of activations were observed in the bilateral insula and overlying opercula, left lateral and right medial orbitofrontal cortex, and the pregenual cingulate cortex, indicating that these regions are reliably and consistently activated in response to gustatory stimulation. The human insula has been associated with the sensory processing of taste, such as the intensity and quality of a taste. It is hence commonly referred to as the primary taste area. The orbitofrontal cortex has been linked to the processing of hedonic aspects of taste processing and is often referred to as the secondary taste area. However, cortical activation patterns change rapidly, within the millisecond time range. Thus, the slow and aggregated hemodynamic measures acquired using functional magnetic resonance imaging and positron emission tomography have clear and inherent problems with providing insights into the dynamics of the early cerebral processing of gustatory stimuli. In order to study how the brain processes taste within the first second after stimulation in healthy humans, one must use either one of two techniques that provide excellent temporal resolution: electroencephalogram or magnetoencephalogram.

This review focuses on the temporal dimension of gustatory processing. For this, we provide a critical overview of over forty years of research on gustatory perception conducted with electroencephalogram or magnetoencephalogram. We will discuss the particular demands on stimulus delivery that result from gustatory electroencephalogram or magnetoencephalogram, and we present a brief overview of the various techniques used to date. We discuss our current knowledge of gustatory event-related brain responses in the context of our understanding of other, nonchemical senses. Moreover, we highlight inconsistencies and gaps in the existing literature.