Enhanced fear and altered neuronal activation in forebrain limbic regions of CX3CR1-deficient mice

Brain Behav Immun. 2018 Feb:68:34-43. doi: 10.1016/j.bbi.2017.09.013. Epub 2017 Sep 22.

Abstract

Mounting evidence supports immune dysfunction in psychiatric conditions such as post-traumatic stress disorder (PTSD). The association of immunomodulatory mechanisms with PTSD-relevant behavior and physiology is not well understood. Communication between neurons and microglia, resident immune cells of the central nervous system, is crucial for optimal regulation of behavior and physiology. In this regard, the fractalkine CX3CL1, secreted from neurons and its target, the microglial CX3CR1 receptor represent a primary neuron-microglia inter-regulatory system important for synaptic plasticity and function. The current study investigated the impact of CX3CR1 deficiency on behaviors relevant to PTSD, such as fear acquisition and memory, acoustic startle response and anxiety-like behavior. Morphological analysis of microglia and neuronal activation within PTSD-relevant forebrain nuclei regulating stress and fear behaviors was also conducted. CX3CR1-deficient (CX3CR1-/-) mice elicited increased fear acquisition as well as reinstatement of fear as compared to wild type (CX3CR1+/+) mice. Conditioned fear and extinction were not significantly different between genotypes. No significant differences were observed in unconditioned acoustic startle response between genotypes. CX3CR1-/- mice showed reduced anxiety-like behaviors as compared with CX3CR1+/+ mice. Morphological assessment of microglia showed region-selective effects of CX3CR1 deficiency, primarily within hypothalamic and cortical areas. Lastly, CX3CR1-/- mice elicited elevated neuronal activity in the PVN and the ventral tegmental-interpeduncular area following reinstatement of fear. Collectively, our data suggest that impaired CX3CR1 function may evoke region-selective alterations in forebrain circuits regulating stress, anxiety and fear, impacting behaviors relevant to disorders such as PTSD.

Keywords: Anxiety; CX3CR1; Fear; Microglia; PTSD; Startle.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Anxiety / metabolism
  • CX3C Chemokine Receptor 1 / genetics*
  • CX3C Chemokine Receptor 1 / metabolism*
  • Chemokine CX3CL1 / genetics
  • Chemokine CX3CL1 / metabolism
  • Disease Models, Animal
  • Fear / physiology*
  • Limbic System / physiology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Microglia / metabolism
  • Neuronal Plasticity / physiology
  • Neurons / physiology
  • Prosencephalon / physiology
  • Reflex, Startle / physiology
  • Stress Disorders, Post-Traumatic / metabolism
  • Stress, Psychological / physiopathology

Substances

  • CX3C Chemokine Receptor 1
  • Chemokine CX3CL1
  • Cx3cl1 protein, mouse
  • Cx3cr1 protein, mouse