Neural Bases of Motivation: Taste, Hunger, and Thirst

Gustatory stimuli are easily specifiable chemicals that elicit reliable ingestion and rejection in many species, and therefore provide a convenient probe for investigating the neural control of the motivated behavior associated with energy, water, and electrolyte regulation. My initial anatomical and electrophysiological research provided the first thorough description of the central gustatory system in any species. Unlike most exteroceptive sensory systems, the gustatory system in rats has more or less direct (dysynaptic) contact with both the thalamo-cortical axis and the limbic system. In fact, the second central gustatory relay in the pontine parabrachial nuclei projects to the thalamic gustatory relay, the hypothalamus, and the amygdala. Subsequent research established that similar pathways also transmit viscerosensory information relayed to the brain over the glossopharyngeal and vagus nerves. Until this complex sensory system had been delineated, research on limbic system mechanisms was hampered by the paucity of direct sensory input or motor output. The only direct way into the limbic system was via the olfactory bulb; the only way out, via the pituitary. Determining the functions and the connections of the parabrachial nuclei has revealed a major route through which sensory information important in autonomic, neuroendocrine, and behavioral responses reach the ventral forebrain.

In a hungry animal, the sensory message resulting from sucrose on the tongue elicits ingestion. In a sated one, the same sensory message can result in rejection. The gastrointestinal events that induce such a switch in behavior include a complex of neural, hormonal, and humoral factors. Primary gustatory axons have their first central synapse in the medulla, as do vagal sensory neurons that contribute some of the gastrointestinal feedback that signals satiety. Ingestion and rejection behaviors themselves are generated by the oral motor nuclei of the medulla and pons. Thus the brainstem includes the sensory, motor, and integrative apparatus necessary to support the rudiments of an important motivated behavior, ingestion. My current research employs anatomical, electrophysiological, and behavioral techniques to analyze the neural components underlying this fundamental behavioral decision, whether to ingest or reject the contents of the oral cavity.

Recently, my laboratory has paid particular attention to characterizing the functions of the brainstem gustatory relay nuclei in awake, behaving rats. This has been accomplished using a combination of lesion-behavioral studies and electrophysiological experiments that test a variety of taste-guided behaviors. We have determined that the gustatory nuclei in the medulla, pons, and thalamus play distinctly different roles in processing taste information. Lesions of the pontine parabrachial nuclei, the second central gustatory relay, block the acquisition of a learned taste aversion and the expression of sodium appetite. Damage to either the first central relay in the medulla or to the thalamic taste area has little or no effect on these behaviors. Because the parabrachial nuclei project to the limbic system, our working hypothesis is that these complex, taste-guided ingestive behaviors are more dependent on this ventral forebrain interaction than on thalamocortical processing.