Abstract
BackgroundThe caudal brainstem plays an important role in short-term satiation and in the control of meal termination. Meal-related stimuli sensed by the gastrointestinal (GI) tract are transmitted to the area postrema (AP) via the bloodstream, or to the nucleus tractus solitarii (NTS) via the vagus nerve. Little is known about the encoding of macronutrient-specific signals in the caudal brainstem. We hypothesized that sucrose and casein peptone activate spatially distinct sub-populations of NTS neurons and thus characterized the latter using statistical three-dimensional modeling.Methodology/Principal FindingsUsing immunolabeling of the proto-oncogene Fos as a marker of neuronal activity, in combination with a statistical three-dimensional modeling approach, we have shown that NTS neurons activated by sucrose or peptone gavage occupy distinct, although partially overlapping, positions. Specifically, when compared to their homologues in peptone-treated mice, three-dimensional models calculated from neuronal density maps following sucrose gavage showed that Fos-positive neurons occupy a more lateral position at the rostral end of the NTS, and a more dorsal position at the caudal end.Conclusion/SignificanceTo our knowledge, this is the first time that subpopulations of NTS neurons have be distinguished according to the spatial organization of their functional response. Such neuronal activity patterns may be of particular relevance to understanding the mechanisms that support the central encoding of signals related to the presence of macronutrients in the GI tract during digestion. Finally, this finding also illustrates the usefulness of statistical three-dimensional modeling to functional neuroanatomical studies.
Highlights
The central nervous system (CNS) controls food intake integrating a broad variety of both environmental and internal inputs [1]
Our findings indicate that macronutrients in the gastrointestinal tract elicit distinct patterns of neuronal activity in the caudal brainstem
Fos-positive neurons were present in sections from all other experimental groups, as illustrated in Figure 2 which shows the number of Fos-positive neurons in the brainstem of mice after water, peptone or sucrose gavage
Summary
The central nervous system (CNS) controls food intake integrating a broad variety of both environmental and internal inputs [1]. During digestion, a complex signaling cascade informs brainstem centers of the nature and quantity of macronutrients entering the organism [1,2]. Both non-specific mechanical and macronutrient-specific meal-related stimuli are sensed in the GI tract, where they induce the release of gut peptides. Within the central nervous system, vagal afferents synapse in the nucleus tractus solitarii (NTS) located in the caudal brainstem. Meal-related stimuli sensed by the gastrointestinal (GI) tract are transmitted to the area postrema (AP) via the bloodstream, or to the nucleus tractus solitarii (NTS) via the vagus nerve. We hypothesized that sucrose and casein peptone activate spatially distinct subpopulations of NTS neurons and characterized the latter using statistical three-dimensional modeling
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