Elevated circulating soluble interleukin-2 receptor (sCD25) level is associated with prefrontal excitatory-inhibitory imbalance in individuals with chronic pain: A proton MRS study

Brain Behav Immun. 2024 Aug:120:1-9. doi: 10.1016/j.bbi.2024.05.020. Epub 2024 May 19.

Abstract

Aberrant neuronal excitability in the anterior cingulate cortex (ACC) is implicated in cognitive and affective pain processing. Such excitability may be amplified by activated circulating immune cells, including T lymphocytes, that interact with the central nervous system. Here, we conducted a study of individuals with chronic pain using magnetic resonance spectroscopy (MRS) to investigate the clinical evidence for the interaction between peripheral immune activation and prefrontal excitatory-inhibitory imbalance. In thirty individuals with chronic musculoskeletal pain, we assessed markers of peripheral immune activation, including soluble interleukin-2 receptor alpha chain (sCD25) levels, as well as brain metabolites, including Glx (glutamate + glutamine) to GABA+ (γ-aminobutyric acid + macromolecules/homocarnosine) ratio in the ACC. We found that the circulating level of sCD25 was associated with prefrontal Glx/GABA+. Greater prefrontal Glx/GABA+ was associated with higher pain catastrophizing, evaluative pain ratings, and anxiodepressive symptoms. Further, the interaction effect of sCD25 and prefrontal Glx/GABA+ on pain catastrophizing was significant, indicating the joint association of these two markers with pain catastrophizing. Our results provide the first evidence suggesting that peripheral T cellular activation, as reflected by elevated circulating sCD25 levels, may be linked to prefrontal excitatory-inhibitory imbalance in individuals with chronic pain. The interaction between these two systems may play a role as a potential mechanism underlying pain catastrophizing. Further prospective and treatment studies are needed to elucidate the specific role of the immune and brain interaction in pain catastrophizing.

Keywords: Anterior cingulate cortex; Chronic pain; GABA; Glutamate; Magnetic resonance spectroscopy; Pain catastrophizing; Soluble interleukin-2 receptor.

MeSH terms

  • Adult
  • Catastrophization / metabolism
  • Chronic Pain* / metabolism
  • Female
  • Glutamic Acid / blood
  • Glutamic Acid / metabolism
  • Glutamine / blood
  • Glutamine / metabolism
  • Gyrus Cinguli / metabolism
  • Humans
  • Interleukin-2 Receptor alpha Subunit* / blood
  • Interleukin-2 Receptor alpha Subunit* / metabolism
  • Male
  • Middle Aged
  • Prefrontal Cortex* / metabolism
  • Proton Magnetic Resonance Spectroscopy
  • gamma-Aminobutyric Acid / metabolism

Substances

  • Interleukin-2 Receptor alpha Subunit
  • Glutamic Acid
  • Glutamine
  • gamma-Aminobutyric Acid
  • IL2RA protein, human