CART neurons in the lateral hypothalamus communicate with the nucleus accumbens shell via glutamatergic neurons in paraventricular thalamic nucleus to modulate reward behavior

Choudhary, Amit; Somalwar, Amita R.; Sagarkar, Sneha; Rale, Abhishek; Sakharkar, Amul J.; Subhedar, Nishikant K.; Kokare, Dadasaheb M.

doi:10.1007/s00429-017-1544-6

Cited by 24 publications

(37 citation statements)

References 78 publications

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“…The orexin/hypocretin fibers originated from the LH can be readily identified in the PVT and are involved in drug seeking and motivated feeding ( Kirouac et al, 2005 ). Cocaine- and amphetamine-regulated transcript (CART) neurons in the LH projecting to the PVT may control food-seeking behavior under natural conditions ( Choudhary et al, 2017 ). An infusion of CART into the PVT attenuates cocaine-primed reinstatement ( James et al, 2010 ).…”

Section: Discussionmentioning

confidence: 99%

Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment

Cheng

Wang

et al. 2018

Front. Mol. Neurosci.

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Foraging food in a novel environment is essential for survival. Animals coordinate the complex motivated states and decide whether to initiate feeding or escape from unfamiliar scenes. Neurons in the paraventricular thalamic nucleus (PVT) receive multiple inputs from the hypothalamus, forebrain, and caudal brainstem that are known to regulate feeding behavior. The PVT neurons also project to the forebrain regions that are involved in reward and motivation. Notably, the PVT neurons projecting to the nucleus accumbens (NAc) are activated when an incentive stimulus is presented. Optogenetic activation of the PVT-NAc path has been shown to increase the motivation for sucrose-seeking in instrumental tasks. However, how the PVT circuitry regulates the feeding behavior in a novel environment remains largely obscure. In the present study, we found that the activity of glutamatergic neurons in the anterior PVT (aPVT) projecting to the NAc dictates the novelty-suppressed feeding behavior in mice. Optogenetic activation of the aPVT-NAc projection increased the feeding time and food consumption in mice under a moderate food restriction in a novel open field where the food was placed in the central area. The exploratory and anxiety-like behaviors, however, were not altered by the aPVT-NAc activation. Our work reveals that activation of the aPVT-NAc pathway in mice generates a motivation to consume food in a novel environment.

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Section: Discussionmentioning

confidence: 99%

Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment

Cheng

Wang

et al. 2018

Front. Mol. Neurosci.

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“…Polysynaptic pathways to the NAc can also modulate reward seeking. For example, LHA CART (cocaine and amphetamine regulated transcript) neurons that project to the paraventricular thalamic nucleus (PVT) promote reward behaviors, which can then be attenuated by glutamate receptor blockade in the NAc shell ( 209 ).…”

Section: Neuronal Inputs To Mesolimbic Pathways That Regulate Homeostmentioning

confidence: 99%

Parallels and Overlap: The Integration of Homeostatic Signals by Mesolimbic Dopamine Neurons

2018

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Motivated behaviors are often initiated in response to perturbations of homeostasis. Indeed, animals and humans have fundamental drives to procure (appetitive behaviors) and eventually ingest (consummatory behaviors) substances based on deficits in body fluid (e.g., thirst) and energy balance (e.g., hunger). Consumption, in turn, reinforces motivated behavior and is therefore considered rewarding. Over the years, the constructs of homeostatic (within the purview of the hypothalamus) and reward (within the purview of mesolimbic circuitry) have been used to describe need-based vs. need-free consumption. However, many experiments have demonstrated that mesolimbic circuits and “higher-order” brain regions are also profoundly influenced by changes to physiological state, which in turn generate behaviors that are poised to maintain homeostasis. Mesolimbic pathways, particularly dopamine neurons of the ventral tegmental area (VTA) and their projections to nucleus accumbens (NAc), can be robustly modulated by a variety of energy balance signals, including post-ingestive feedback relaying nutrient content and hormonal signals reflecting hunger and satiety. Moreover, physiological states can also impact VTA-NAc responses to non-nutritive rewards, such as drugs of abuse. Coupled with recent evidence showing hypothalamic structures are modulated in anticipation of replenished need, classic boundaries between circuits that convey perturbations in homeostasis and those that drive motivated behavior are being questioned. In the current review, we examine data that have revealed the importance of mesolimbic dopamine neurons and their downstream pathways as a dynamic neurobiological mechanism that provides an interface between physiological state, perturbations to homeostasis, and reward-seeking behaviors.

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“…Several lines of evidence can be found in the realm of expert’s practice and relevant scientific literature. For example, the NAc/ventral striatum of the accumbal macrosystem drives and reinforces reward-associated feeding and sexual or somatic and visceral (loco)motor actions, including repetitive behavior [20, 32, 35, 42, 43, 55, 66, 73, 90, 98, 99, 106, 117, 173, 214, 232, 244]. Motivations, shaping the emotional [76] or cognitive addiction behavior [81, 83, 190, 196] via activating the NAc-hippocampus and hypothalamus-NAc circuits, respectively, have the potential of alternative execution as well.…”

Section: The Macrosystem Nac—from Motivation To Actionmentioning

confidence: 99%

Molecular Plasticity of the Nucleus Accumbens Revisited—Astrocytic Waves Shall Rise

et al. 2019

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Part of the ventral striatal division, the nucleus accumbens (NAc) drives the circuit activity of an entire macrosystem about reward like a “flagship,” signaling and leading diverse conducts. Accordingly, NAc neurons feature complex inhibitory phenotypes that assemble to process circuit inputs and generate outputs by exploiting specific arrays of opposite and/or parallel neurotransmitters, neuromodulatory peptides. The resulting complex combinations enable versatile yet specific forms of accumbal circuit plasticity, including maladaptive behaviors. Although reward signaling and behavior are elaborately linked to neuronal circuit activities, it is plausible to propose whether these neuronal ensembles and synaptic islands can be directly controlled by astrocytes, a powerful modulator of neuronal activity. Pioneering studies showed that astrocytes in the NAc sense citrate cycle metabolites and/or ATP and may induce recurrent activation. We argue that the astrocytic calcium, GABA, and Glu signaling and altered sodium and chloride dynamics fundamentally shape metaplasticity by providing active regulatory roles in the synapse- and network-level flexibility of the NAc.

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CART neurons in the lateral hypothalamus communicate with the nucleus accumbens shell via glutamatergic neurons in paraventricular thalamic nucleus to modulate reward behavior

Cited by 24 publications

References 78 publications

Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment

Anterior Paraventricular Thalamus to Nucleus Accumbens Projection Is Involved in Feeding Behavior in a Novel Environment

Parallels and Overlap: The Integration of Homeostatic Signals by Mesolimbic Dopamine Neurons

Molecular Plasticity of the Nucleus Accumbens Revisited—Astrocytic Waves Shall Rise

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