Neural Ensemble Recordings from Central Gustatory-Reward Pathways in Awake and Behaving Animals

The mammalian gustatory system participates in the detection and discrimination of intraoral stimuli, allowing for the selection of nutrients and rejection of toxic compounds. However, the sensory percept of a substance that is placed in the mouth does not depend solely on its taste. The olfactory and somatosensory systems discriminate odor, texture, and temperature, which participate, with taste, in the unitary perception of flavor (Small and Prescott 2005). Flavor is a central contributor in the decision making relative to ingestive behavior. However, feeding decisions are made in specific physiological contexts and, therefore, are not entirely dependent on sensory experience. We know today that the central nervous system (CNS) detects a multitude of peripheral neural and humoral signals that reflect gastrointestinal status and current energy needs, availability, and stores (Broberger 2005). The regulation of energy homeostasis and maintenance of stable body weight depend on the integration of these signals and the ability to respond adequately through the modulation of both energy expenditure and food intake (Schwartz and Porte 2005). The appearance and familiarity of a particular food, given the memory of the orosensory, olfactory, and postingestive (Garcia, Kimeldorf et al. 1955; Sclafani 2004) effects of previously encountered identical or similar substances, will also influence the decision of ingestion, as will emotional, cognitive, and social factors (Wilson 2002). These observations underline that, when trying to understand food seeking, one should consider not only sensory and homeostatic factors but others such as emotional processing, learning and decision making (Balleine 2005; Kelley, Baldo et al. 2005). Data obtained by recording neural ensemble activity in awake animals has demonstrated not only that neural populations distributed across several cortical and subcortical brain areas can encode the multisensory properties of intraoral stimuli but also that this coding is modulated by physiological state (de Araujo, Gutierrez et al. 2006; Fontanini and Katz 2006; Gutierrez, Carmena et al. 2006; Stapleton, Lavine et al. 2006). Consequently, it has been proposed that gustatory processing must be considered in a multimodal perspective, combining taste with the several other sensory and homeostatic processes that occur in association with taste receptor activation (Jones, Fontanini et al. 2006; Simon, de Araujo et al. 2006). According to this view, gustation results from a distributed neural process by which information conveyed to the brain through specialized taste, and oral somatosensory, olfactory, and gastrointestinal fibers is integrated with humoral signals, allowing the organism to feed in accordance with the maintenance of adequate energy homeostasis, and participating with complex neural circuits of affective and cognitive processing to organize ingestive behavior. In our laboratories at Duke University, experimental work is directed to further understand the neural mechanisms of gustation in order to contribute towards a better comprehension of dysfunctional feeding behavior, especially as it relates to hyperphagia and obesity. In this chapter we will describe the methodology currently in use in our laboratories to perform neural ensemble recordings from the gustatory-reward system of awake and freely licking mice and rats, as well as other associated measures performed simultaneously or in parallel to neural recordings.