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Differential role of anterior cingulate cortical glutamatergic neurons in pain-related aversion learning and nociceptive behaviors in male and female rats
Jarrin, Sarah; Pandit, Abhay; Roche, Michelle; Finn, David P.
Pain is comprised of both sensory and affective components. The anterior cingulate cortex (ACC) is a key brain region involved in the emotional processing of pain. Specifically, glutamatergic transmission within the ACC has been shown to modulate pain-related aversion. In the present study, we usein vivooptogenetics to activate or silence, using channelrhodopsin (ChR2) and archaerhodopsin (ArchT) respectively, calmodulin-kinase II alpha (CaMKII alpha)-expressing excitatory glutamatergic neurons of the ACC during a formalin-induced conditioned place aversion (F-CPA) behavioral paradigm in both female and male adult Sprague-Dawley rats. Expression of c-Fos, a marker of neuronal activity, was assessed within the ACC using immunohistochemistry. Optogenetic inhibition of glutamatergic neurons of the ACC abolished F-CPA without affecting formalin-induced nociceptive behavior during conditioning. In male rats, optogenetic activation of ACC glutamatergic neurons decreased formalin-induced nociceptive behavior during conditioning without affecting F-CPA. Interestingly, the opposite effect was seen in females, where optogenetic activation of glutamatergic neurons of the ACC increased formalin-induced nociceptive behavior during conditioning. The abolition of F-CPA following optogenetic inhibition of glutamatergic neurons of the ACC was associated with a reduction in c-Fos immunoreactivity in the ACC in male rats, but not female rats. These results suggest that excitatory glutamatergic neurons of the ACC play differential and sex-dependent roles in the aversion learning and acute sensory components of pain. This work was supported by financial support from Science Foundation Ireland (SFI) and co-funded under the European Regional Development Fund under Grant Number 13/RC/2073. The funders played no part in study design, in the collection, analysis and interpretation of data, in the writing of the report or in the decision to submit the article for publication.
Keyword(s): anterior cingulate cortex; glutamate neurons; optogenetics; inflammatory pain; formalin; rat; c-Fos; conditioned place aversion; SEX-DIFFERENCES; ANXIETY DISORDERS; AFFECTIVE COMPONENT; CORTEX CONTRIBUTES; NEUROPATHIC PAIN; COMORBIDITY; ACTIVATION; INHIBITION; ANTAGONISM; MODULATION
Publication Date:
2020
Type: Journal article
Peer-Reviewed: Yes
Language(s): English
Contributor(s): Science Foundation Ireland; European Regional Development Fund
Institution: NUI Galway
Publisher(s): Frontiers Media
File Format(s): application/pdf
First Indexed: 2020-11-04 06:31:32 Last Updated: 2020-11-04 06:31:32