Anatomical Organization and Coding in the Gustatory System: A Functional Perspective

Abstract

Gustatory signals from the mouth travel to the rostral nucleus of the solitary tract (rNST) over the VIIth (anterior tongue and palate) and IXth (posterior tongue) cranial nerves and synapse in the central subdivision in an overlapping orotopic pattern. Oral somatosensory information likewise reaches rNST, preferentially terminating in the lateral subdivision. Two additional rNST subdivisions, the medial and ventral, receive only sparse primary afferent inputs. Ascending pathways arise primarily from the central subdivision; local reflex and intranuclear pathways originate from the other subdivisions. Thus, parallel processing is already evident at the first central nervous system (CNS) relay. Ascending rNST taste fibers connect to the pontine parabrachial nucleus (PBN), strongly terminating in the ventral lateral (VL) and medial subnuclei (M) of the waist region but also in the external lateral (EL) and medial (EM) subnuclei. PBN projections travel along two main routes. A “lemniscal” processing stream connects to the thalamic taste relay, the parvicellular division of the ventroposteromedial nucleus (VPMpc), which in turn projects to insular cortex. A second, “limbic” pathway synapses in the lateral hypothalamus (LH), central nucleus of the amygdala (CeA), bed nucleus of the stria terminalis (BNST), and substantia innominata (SI). The ventral tegmental area (VTA), a critical nucleus in the so-called reward circuit, also receives input from the gustatory PBN. Forebrain gustatory structures are interconnected and give rise to copious feedback pathways. Single-neuron recording and calcium imaging demonstrates that taste response profiles in both the peripheral nerves and CNS lemniscal structures are highly orderly. Arguably, a limited number of neuron “types” are defined by the qualitative class of compounds (sugars, sweeteners, amino acids, sodium salts, acids and non-sodium salts, “bitter”) that elicit the largest response in a cell. In the periphery and NST, some findings suggest these classes correspond to distinct molecular phenotypes and functions, but evidence for a cortical chemotopic organization is highly controversial. CNS neuron types are complicated by convergence and lability as a function of homeostatic, cognitive, and experiential variables. Moreover, gustatory responses are dynamic, providing additional coding potential in the temporal domain. Interestingly, taste responses in the limbic pathway are particularly plastic and code for hedonics more obviously than quality. Studies in decerebrate rats reveal that the brainstem is sufficient to maintain appropriate oromotor and somatic responses, referred to as taste reactivity, to nutritive (sugars) and harmful (quinine) stimuli. However, forebrain processing is necessary for taste reactivity to be modulated by learning, at least with respect to taste aversion conditioning. Functional studies of the rodent cortex tell a complex story. Lesion studies in rats emphasize a considerable degree of residual function in animals lacking large regions of insular cortex despite demonstrating shifts in detection thresholds for certain, but not all, stimuli representing different taste qualities. They also have an impact on conditioned taste aversion. Investigations in mice employing optogenetic and chemogenetic manipulations suggest that different regions of insular cortex are critical for discriminating certain qualities and that their connections to the amygdala underlie their hedonic impact. The continued use of sophisticated behavioral experiments coordinated with molecular methods for monitoring and manipulating activity in defined neural circuits should ultimately yield satisfying answers to long-standing debates about the fundamental operation of the gustatory system.