While gustation in the hamster has been extensively studied at the behavioral and physiological level, very little is known about the central anatomy of the taste system. The purpose of this study was to trace the connections of the parabrachial nucleus (PBN) in the golden Syrian hamster (Mesocricetus auratus) using wheat germ agglutinin-conjugated horseradish peroxidase. The PBN is the site of the second central synapse for the ascending gustatory system and receives taste afferents from the nucleus of the solitary tract. Following large injections into the PBN, anterogradely transported label was seen in the lateral hypothalamus, dorsal thalamus, bed nucleus of the stria terminalis, and amygdala. The anatomy of the two primary targets, the ventral posteromedial thalamus and central nucleus of the amygdala, is described based on Nissl-stained material, and acetylcholinesterase and NADH dehydrogenase histochemistry. Injections into these two regions revealed different patterns of efferents within the PBN. Following injections into the thalamus, retrogradely labelled cell bodies were distributed throughout the PBN subdivisions bilaterally, but concentrated in the central medial (CM) and external lateral (EL) subdivisions. Following injections into the amygdala, retrogradely labelled cell bodies were primarily in the ipsilateral PBN EL, while anterogradely transported label was distributed throughout much of the ipsilateral PBN. The majority of CM efferents projecting to the thalamus were elongate cells, whereas the majority of CM efferents to the amygdala were round-oval cells. These results indicate that the ascending central gustatory system changes from a serial pathway (nucleus of the solitary tract-PBN) to a parallel organization consisting of two major projections, the parabrachio-thalamo-cortical and parabrachio-amygdaloid pathways.
The responses of single parabrachial nucleus (PBN) neurons were recorded extracellularly to characterize their sensitivity to stimulation of individual gustatory receptor subpopulations (G neurons, n = 75) or mechanical stimulation of defined oral regions (M neurons, n = 54) then localized to morphologically defined PBN subdivisions. Convergence from separate oral regions onto single neurons occurred frequently for both G and M neurons, but converging influences were more potent when they arose from nearby locations confined to the anterior (AO) or posterior oral cavity (PO). A greater number of G neurons responded optimally to stimulation of AO than to PO receptor subpopulations, and these AO-best G neurons had higher spontaneous and evoked response rates but were less likely to receive convergent input than PO-best G neurons. In contrast, proportions, response rates, and convergence patterns of AO- and PO-best M neurons were more comparable. The differential sensitivity of taste receptor subpopulations was reflected in PBN responses. AO stimulation with NaCl elicited larger responses than PO stimulation; the converse was true for QHCl stimulation. Within the AO, NaCl elicited a larger response when applied to the anterior tongue than to the nasoincisor duct. Hierarchical cluster analysis of chemosensitive response profiles suggested two groups of PBN G neurons. One group was composed of neurons optimally responsive to NaCl (N cluster); the other to HCl (H cluster). Most N- and H-cluster neurons were AO-best. Although they were more heterogenous, all but one of the remaining G neurons were unique in responding best or second-best to quinine and so were designated as quinine sensitive (Q+). Twice as many Q+ neurons were PO- compared with AO-best. M neurons were scattered across PBN subdivisions, but G neurons were concentrated in two pairs of subdivisions. The central medial and ventral lateral subdivisions contained both G and M neurons but were dominated by AO-best N-cluster G neurons. The distribution of G neurons in these subdivisions appeared similar to distributions in most previous studies of PBN gustatory neurons. In contrast to earlier studies, however, the external medial and external lateral-inner subdivisions also contained G neurons, intermingled with a comparable population of M neurons. Unlike cells in the central medial and ventral lateral subnuclei, nearly every neuron in the external subnuclei was PO best, and only one was an N-cluster cell. In conclusion, the present study supports a functional distinction between sensory input from the AO and PO at the pontine level, which may represent an organizing principle throughout the gustatory neuraxis. Furthermore, two morphologically distinct pontine regions containing orosensory neurons are described.
The locations of taste-responsive areas within the brainstem parabrachial nucleus (PBN), an obligatory taste relay in the golden hamster (Mesocricetus auratus), were mapped in relation to cytoarchitectural boundaries. The PBN was systematically searched for multiunit neural activity in response to a taste mixture composed of 0.1 M sucrose, 0.03 M NaCl, and 0.1 M KCl applied to the anterior tongue. Taste responses were located exclusively in one of three subdivisions of the medial PBN, which is thought to be specialized for gustatory processing, and in one of six subdivisions of the lateral PBN, which is thought to be specialized for general visceral processing. Based on Nissl-stained material, both the medial and lateral PBN subdivisions in the hamster were similar to those reported for the rat PBN. The largest group of taste-responsive cells encompassed two-thirds of the central medial subdivision, while a smaller group of taste cells was exclusively located within the ventral lateral subdivision. The two taste-responsive subdivisions are separated by the superior cerebellar peduncle and contain diverse cell types. The finding that anterior tongue taste may be exclusively represented in circumscribed cytoarchitecturally defined parts of two PBN divisions suggests that taste information from the anterior tongue is required for both specific gustatory and general visceral functions.
The orosensory nucleus of the solitary tract (NST) receives input from the amygdala, a key node in the forebrain feeding-related network. Despite numerous studies documenting the existence of this pathway, however, too little is known about the input organization to the gustatory brainstem to allow definitive conclusions about its functional role. Therefore, towards the long-term goal of characterizing such descending regulatory pathways, the purpose of the present study was to describe the distribution of input arising from the amygdala. The anterograde tracer, biotinylated dextran, was injected into the central amygdala based on stereotaxic coordinates in seven adult male rats. Following a 2-week survival time, the animals were sacrificed. Transverse sections of the brains were processed to visualize transported tracer and NST anatomical topography. Labeled fibers were differentially distributed among subdivisions throughout the rostrocaudal extent of NST. Within the rostral NST, the medial (M) subdivision had the highest density of terminal-like endings and swellings (30% of total density), followed by the ventral half of rostral central (vRC, 29%), ventral (V, 25%), dorsal half of rostral central (dRC, 12%) and rostral lateral (RL, 4%). In conclusion, it appears that amygdalar input preferentially overlaps with NST subdivisions (M, V, vRC) containing neurons with local efferent projections to the caudal NST and reticular nuclei that are implicated in medullary reflex circuits, rather than with subdivisions (dRC, RL) receiving primary orosensory afferent input and containing neurons having ascending efferent projections to the parabrachial nucleus. Thus, descending feeding-related pathways may be positioned to act as regulatory substrates controlling the output gain of brainstem circuits which may serve to modulate sensorimotor and autonomic reflexes in response to ingestive behaviors.
The distribution of acetylcholinesterase (AChE), NADH dehydrogenase (NADHd), and cytochrome oxidase (CO) was determined in the nucleus of the solitary tract (NST) in the golden hamster. Histochemical staining was compared to cytoarchitectonic subdivisions of the NST (Whitehead: J. Comp. Neurol. 276:547-572, 1988) and to terminal fields of primary afferents of the nerves that innervate the tongue. These three histochemical methods resulted in differential staining patterns within the NST that were related to certain subdivisions. Transganglionic transport of horseradish peroxidase (HRP) was used to determine the central projections of the chorda tympani (CT), the lingual branch of the trigeminal (L-V), and the lingual-tonsilar branch of the glossopharyngeal nerves (L-IX). Alternate or the same brain sections were processed to reveal transported HRP, and NADHd or AChE levels. Increased staining of the neuropil with NADHd and AChE was coincident with the dense part of the afferent terminal fields of all three nerves in the NST and the laterally adjacent dorsomedial part of the spinal trigeminal nucleus. CO showed this pattern only for the most rostral part of the CT field. The densest AChE staining coincided with gustatory afferent terminal fields. The histochemical staining facilitated the interpretation of the organization of the NST. For example, at caudal levels of the gustatory NST, it is suggested that taste processing is localized predominantly in the medial part of the rostral central, and somatosensory processing in the rostral lateral subdivision. AChE or NADHd staining should facilitate studies of connections, topography, and neuroplastic changes of the gustatory NST.
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