Taste pathways to hypothalamus and amygdala

Abstract

The projections of a third order gustatory relay in the dorsal pons of rats have been traced using tritiated proline autoradiography and antidromic activation of pontine neurons from electrodes in the thalamus and amygdala. Labelled axons collect in the central tegmental tract and ascend to the thalamic taste area in the medial extension of the ventrobasal complex. The majority of the fibers remain ipsilateral, but a few cross in the rostral pons and midbrain. The largest crossing occurs at the level of the thalamic termination. Many fascicles of fibers continue rostrally by passing beneath the thalamic taste area, piercing the medial lemniscus, and spreading out along the dorsomedial corner of the internal capsule (IC). The terminal field at this level caps IC from the subthalamic nucleus down into the far-lateral hypothalamus. Labelled axons grandually penetrate through the internal capsule, and ramify throughout the underlying substantia innominata. This terminal zone extends laterally into the rostral end of the central nucleus of the amygdala, which is densely labelled to its caudal exremity. At the caudal end of the amygdala labelled fibers are visible in one component of the stria terminalis. These fibers can be followed over the dorsal thalamus into a smaller, but equally dense terminal area in the dorsolateral bed nucleus of the stria terminalis. The electrophysiological data demonstrate that pontine gustatory units can be antidromically activated by electrodes located in or near the central nucleus of the amygdala. Since many of the same units can also be driven from the thalamic taste area, at least some of the axons traced autoradiographically probably convey gustatory information to the hypothalamus and amygdala.

The gustatory neocortex of the rat

“…Anatomical and electrophysiological observations of relationships between the gustatory thalamus and the GN, the somatosensory system (Burton & Benjamin, 1971;Scott & Erickson, 1971), the olfactory system (Giachetti & MacLeod, 1977;Powell, Cowan, & Raisman, 1965), the hypothalamus (Emmers, 1977;Norgren, 1976), and pontine taste area (see Norgren, 1977) suggest the thalamus as a focus for the expression of taste behavior symptoms following other forebrain lesions. However, the apparent neutralization of hedonic preferences and aversions to taste stimuli following thalamic lesions (Ables & Benjamin, 1960;Oakley & Pfaffmann, 1962), an effect that is not at all apparent following either GN ablation or decerebration, suggests the presence of a second focus in addition to the ventrobasal thalamus.…”

“…Axonal transport studies have shown that the SOL contains somata and/or axons of passage which project to the marginal parabrachial nuclei, central nucleus of the amygdala (CE), the subthalamic nuclei (CN), substantia innominata (SI), anterior hypothalamus (AH), and the bed nucleus of stria terminalis (BST) (Norgren, 1976(Norgren, , 1978Ricardo & Koh, 1978). Such findings have served to implicate these projection pathways in gustatory function.…”

“…However, adequate verification of gustatory responses within these areas has not yet been provided, and anatomical as well as electrophysiological observations suggest that these basal forebrain regions may be preferentially involved in the relay of visceral (gastrointestinal) information rather than of taste information per se (see Norgren, 1968;Ricardo & Koh, 1978;Voshort & Van der Kooy, 1981). Ricardo and Koh (1978) showed that injections of tritiated amino acids into caudal portions of the SOL, which are posterior to gustatory-responsive areas (see Norgren, 1976Norgren, , 1978, also result in labeling within the CE, SI, BST, and AR It seems likely, then, that forebrain labeling within these areas following injections within the rostral SOL involves gustatory as well as visceral projections (Norgren, 1978). It is clear, however, based upon electrophysiological observations by many investigators, that gustatory afferents do synapse within the PTA (e.g., Norgren, 1974;Norgren & Pfaffmann, 1975;Perrotto & Scott, 1976;Scott & Perrotto, 1980).…”

Transient expression of c-Fos in rat amygdala during training is required for encoding conditioned taste aversion memory.

“…1994). It is also supported by the neuroanatomical links of the amygdala to other brain areas implicated in CTA, including the NTS, PBN, thalamus, and insular cortex (Norgren 1976;van der Kooy et al 1984;Turner and Hrekenham 1991), and by the role assigned to the amygdala in other types of learning, especially aversive and emotional conditioning (Davis 1992;LeDoux 1993;McGaugh ct al. 1993;Cahill et al 1995).…”

Convergence of sensory systems in the orbitofrontal cortex in primates and brain design for emotion

“…Interestingly, there appears to have been a major change in phylogeny in the connections of the taste pathways, in that in rodents the first central relay, the nucleus of the solitary tract, connects to a pontine taste area, which sends projections directly to subcortical structures such as the amygdala and hypothalamus. In contrast, in primates there appears to be no pontine taste area; instead, there is obligatory connectivity from the nucleus of the solitary tract to the taste thalamus and thus to the primary taste cortex in the anterior insula and adjoining frontal operculum (Norgren and Leonard, 1973;Norgren, 1976Norgren, , 1984. This fundamental difference in the anatomy of the rodent and primate taste pathways shows that even Fig.…”