Hindbrain catecholaminergic inputs to the paraventricular thalamus scale feeding and metabolic efficiency in stress‐related contexts

Abstract

The regulation of food intake and energy balance relies on the dynamic integration of exteroceptive and interoceptive signals monitoring nutritional, metabolic, cognitive, and emotional states. The paraventricular thalamus (PVT) is a central hub that, by integrating sensory, metabolic, and emotional states, may contribute to the regulation of feeding and homeostatic/allostatic processes. However, the underlying PVT circuits still remain elusive. Here, we aimed at unravelling the role of catecholaminergic (CA) inputs to the PVT in scaling feeding and metabolic efficiency. First, using region‐specific retrograde disruption of CA projections, we show that PVT CA inputs mainly arise from the hindbrain, notably the locus coeruleus (LC) and the nucleus tractus solitarius. Second, taking advantage of integrative calorimetric measurements of metabolic efficiency, we reveal that CA inputs to the PVT scale adaptive feeding and metabolic responses in environmental, behavioural, physiological, and metabolic stress‐like contexts. Third, we show that hindbrainTH→PVT inputs contribute to modulating the activity of PVT as well as lateral and dorsomedial hypothalamic neurons. In conclusion, the present study, by assessing the key role of CA inputs to the PVT in scaling homeostatic/allostatic regulations of feeding patterns, reveals the integrative and converging hindbrainTH→PVT paths that contribute to whole‐body metabolic adaptations in stress‐like contexts. Key points The paraventricular thalamus (PVT) is known to receive projections from the hindbrain. Here, we confirm and further extend current knowledge on the existence of hindbrainTH→PVT catecholaminergic inputs, notably from the locus coeruleus and the nucleus tractus solitarius, with the nucleus tractus solitarius representing the main source. Disruption of hindbrainTH→PVT inputs contributes to the modulation of PVT neuron activity. HindbrainTH→PVT inputs scale feeding strategies in environmental, behavioural, physiological, and metabolic stress‐like contexts. HindbrainTH→PVT inputs participate in regulating metabolic efficiency and nutrient partitioning in stress‐like contexts. HindbrainTH→PVT inputs, directly and/or indirectly, contribute to modulating the downstream activity of lateral and dorsomedial hypothalamic neurons.

Perioperative sleep deprivation activates the paraventricular thalamic nucleus resulting in persistent postoperative incisional pain in mice

“…This suggests that the PVT primarily regulates negative emotions by receiving signals from the brain stem. In addition, the PVT regulates negative emotions by integrating the mPFC cognitive signals and internal state signals of the hypothalamus and brainstem (Christoffel et al, 2021;Dumont et al, 2022Dumont et al, ). 10.3389/fnana.2022 In other words, the PVT integrates corresponding signal inputs and play the role of descending facilitatory system.…”

The gut-brain vagal axis scales hippocampal memory processes and plasticity

“…lung, heart, gut). Vagal afferents-conveyed sensory information is processed and integrated by neurons harbored within the brainstem region of the nucleus of the tractus solitarius (NTS) which in turn projects to a variety of downstream brain regions (Dumont et al, 2022; Gasparini et al, 2020; He et al, 2022; Roman et al, 2016; Trapp and Cork, 2015), therefore contributing to the establishment of extensive interoception-related neuronal networks.…”

Mapping of afferent and efferent connections of phenylethanolamine N‐methyltransferase‐expressing neurons in the nucleus tractus solitarii

“… 3 The NTS not only integrates information from peripheral receptors, but also receives inputs from central nervous systems, such as brainstem, 4 hypothalamus, 5 and limbic system. 6 Meanwhile, NTS neurons extend their axons to numerous brain regions, 7 , 8 , 9 endowing the NTS with the remarkable ability to modulate multiple physiological functions. In addition to regulating cardiopulmonary activity, 2 , 9 compelling evidence has also linked NTS neurons to the regulation of sleep, 10 feeding 11 and anorexia.…”