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GABAergic basal forebrain projections to the periaqueductal gray promote food consumption, reward and predation.

ABSTRACT: Behaviors central to the procurement and consumption of food are among those most fundamental to survival, but their inappropriate expression can lead to overeating and obesity. Nevertheless, we have a poor understanding of circuits that promote feeding independent of physiological demand. Here we demonstrate that activation of basal forebrain (BF) GABAergic neurons results in consumption of food as well as non-food items in well-fed mice, and performance of fictive eating in the absence of ingestible materials. In addition, stimulation of these cells disrupts defensive threat responses and elicits reward-like motivational effects. Finally, BF GABAergic activity triggers skilled predatory attacks of live prey and prey-like objects, but not social targets. These effects were entirely recapitulated by selective stimulation of BF GABAergic projections to the periaqueductal gray (PAG). Our results outline a potent circuit mechanism for increased feeding through recruitment of distinct but synergistic behaviors, and add to growing evidence that PAG is an important integrator of feeding-related activity.

SUBMITTER: Roman-Ortiz C

PROVIDER: S-EPMC8608827 | biostudies-literature | 2021 Nov

REPOSITORIES: biostudies-literature

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GABAergic basal forebrain projections to the periaqueductal gray promote food consumption, reward and predation.

Roman-Ortiz Ciorana C Guevara Jessica A JA Clem Roger L RL

Scientific reports 20211122 1

Behaviors central to the procurement and consumption of food are among those most fundamental to survival, but their inappropriate expression can lead to overeating and obesity. Nevertheless, we have a poor understanding of circuits that promote feeding independent of physiological demand. Here we demonstrate that activation of basal forebrain (BF) GABAergic neurons results in consumption of food as well as non-food items in well-fed mice, and performance of fictive eating in the absence of inge ...[more]

PMID: 34811442

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Project description:Neuroimmune signaling is increasingly identified as a critical component of various illnesses, including chronic pain, substance use disorder, and depression. However, the underlying neural mechanisms remain unclear. Proinflammatory cytokines, such as tumor necrosis factor-α (TNF-α), may play a role by modulating synaptic function and long-term plasticity. The midbrain structure periaqueductal gray (PAG) plays a well-established role in pain processing, and although TNF-α inhibitors have emerged as a therapeutic strategy for pain-related disorders, the impact of TNF-α on PAG neuronal activity has not been thoroughly characterized. Recent studies have identified subpopulations of ventrolateral PAG (vlPAG) with opposing effects on nociception, with dopamine (DA) neurons driving pain relief in contrast to GABA neurons. Therefore, we used slice physiology to examine the impact of TNF-α on neuronal activity of both these subpopulations. We focused on female mice since the PAG is a sexually dimorphic region and most studies use male subjects, limiting our understanding of mechanistic variations in females. We selectively targeted GABA and DA neurons using transgenic reporter lines. Following exposure to TNF-α, there was an increase in excitability of GABA neurons along with a reduction in glutamatergic synaptic transmission. In DA neurons, TNF-α exposure resulted in a robust decrease in excitability along with a modest reduction in glutamatergic synaptic transmission. Interestingly, TNF-α had no effect on inhibitory transmission onto DA neurons. Collectively, these data suggest that TNF-α differentially affects the function of GABA and DA neurons in female mice and enhances our understanding of how TNF-α-mediated signaling modulates vlPAG function.NEW & NOTEWORTHY This study describes the effects of TNF-α on two distinct subpopulations of neurons in the vlPAG. We show that TNF-α alters both neuronal excitability and glutamatergic synaptic transmission on GABA and dopamine neurons within the vlPAG of female mice. This provides critical new information on the role of TNF-α in the potential modulation of pain, since activation of vlPAG GABA neurons drives nociception, whereas activation of dopamine neurons drives analgesia.

Dataset Information

GABAergic basal forebrain projections to the periaqueductal gray promote food consumption, reward and predation.

Publications

GABAergic basal forebrain projections to the periaqueductal gray promote food consumption, reward and predation.

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