Increased intrinsic and synaptic excitability of hypothalamic POMC neurons underlies chronic stress-induced behavioral deficits

Mol Psychiatry. 2023 Mar;28(3):1365-1382. doi: 10.1038/s41380-022-01872-5. Epub 2022 Dec 6.

Abstract

Chronic stress exposure induces maladaptive behavioral responses and increases susceptibility to neuropsychiatric conditions. However, specific neuronal populations and circuits that are highly sensitive to stress and trigger maladaptive behavioral responses remain to be identified. Here we investigate the patterns of spontaneous activity of proopiomelanocortin (POMC) neurons in the arcuate nucleus (ARC) of the hypothalamus following exposure to chronic unpredictable stress (CUS) for 10 days, a stress paradigm used to induce behavioral deficits such as anhedonia and behavioral despair [1, 2]. CUS exposure increased spontaneous firing of POMC neurons in both male and female mice, attributable to reduced GABA-mediated synaptic inhibition and increased intrinsic neuronal excitability. While acute activation of POMC neurons failed to induce behavioral changes in non-stressed mice of both sexes, subacute (3 days) and chronic (10 days) repeated activation of POMC neurons was sufficient to induce anhedonia and behavioral despair in males but not females under non-stress conditions. Acute activation of POMC neurons promoted susceptibility to subthreshold unpredictable stress in both male and female mice. Conversely, acute inhibition of POMC neurons was sufficient to reverse CUS-induced anhedonia and behavioral despair in both sexes. Collectively, these results indicate that chronic stress induces both synaptic and intrinsic plasticity of POMC neurons, leading to neuronal hyperactivity. Our findings suggest that POMC neuron dysfunction drives chronic stress-related behavioral deficits.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acute Disease
  • Anhedonia* / physiology
  • Animals
  • Arcuate Nucleus of Hypothalamus* / metabolism
  • Arcuate Nucleus of Hypothalamus* / physiopathology
  • Cerebral Cortex / metabolism
  • Cerebral Cortex / physiopathology
  • Chronic Disease
  • Cortical Excitability / physiology
  • Depression* / metabolism
  • Depression* / physiopathology
  • Disease Models, Animal
  • Female
  • Male
  • Mental Disorders / metabolism
  • Mental Disorders / physiopathology
  • Mice
  • Mice, Inbred C57BL
  • Nervous System Physiological Phenomena
  • Neuronal Plasticity / physiology
  • Neurons* / metabolism
  • Neurons* / physiology
  • Pro-Opiomelanocortin* / biosynthesis
  • Pro-Opiomelanocortin* / metabolism
  • Stress, Psychological* / metabolism
  • Stress, Psychological* / physiopathology
  • Synapses / metabolism
  • Synapses / physiology

Substances

  • Pro-Opiomelanocortin