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Visceral hypersensitivity induced by optogenetic activation of the amygdala in conscious rats.

Abstract

In vivo optogenetics identifies brain circuits controlling behaviors in conscious animals by using light to alter neuronal function and offers a novel tool to study the brain-gut axis. Using adenoviral-mediated expression, we aimed to investigate whether photoactivation with channelrhodopsin (ChR2) or photoinhibition with halorhodopsin (HR3.0) of fibers originating from the central nucleus of the amygdala (CeA) at the bed nucleus of the stria terminalis (BNST) had any effect on colonic sensitivity. We also investigated whether there was any deleterious effect of the adenovirus on the neuronal population or the neuronal phenotype within the CeA-BNST circuitry activated during the optogenetic stimulation. In male rats, the CeA was infected with vectors expressing ChR2 or HR3.0 and fiber optic cannulae were implanted on the BNST. After 8-10 wk, the response to graded, isobaric colonic distension was measured with and without laser stimulation of CeA fibers at the BNST. Immunohistochemistry and histology were used to evaluate vector expression, neuronal integrity, and neurochemical phenotype. Photoactivation of CeA fibers at the BNST with ChR2 induced colonic hypersensitivity, whereas photoinhibition of CeA fibers at the BNST with HR3.0 had no effect on colonic sensitivity. Control groups treated with virus expressing reporter proteins showed no abnormalities in neuronal morphology, neuronal number, or neurochemical phenotype following laser stimulation. Our experimental findings reveal that optogenetic activation of discrete brain nuclei can be used to advance our understanding of complex visceral nociceptive circuitry in a freely moving rat model. NEW & NOTEWORTHY Our findings reveal that optogenetic technology can be employed as a tool to advance understanding of the brain-gut axis. Using adenoviral-mediated expression of opsins, which were activated by laser light and targeted by fiber optic cannulae, we examined central nociceptive circuits mediating visceral pain in a freely moving rat. Photoactivation of amygdala fibers in the stria terminalis with channelrhodopsin induced colonic hypersensitivity, whereas inhibition of the same fibers with halorhodopsin did not alter colonic sensitivity.

Authors+Show Affiliations

Oklahoma Center for Neuroscience , Oklahoma City, Oklahoma.Oklahoma Center for Neuroscience , Oklahoma City, Oklahoma.Oklahoma Center for Neuroscience , Oklahoma City, Oklahoma.Department of Veterans Affairs Medical Center , Oklahoma City, Oklahoma. Oklahoma Center for Neuroscience , Oklahoma City, Oklahoma. Department of Physiology, University of Oklahoma Health Sciences Center , Oklahoma City, Oklahoma.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

29351398

Citation

Johnson, Anthony C., et al. "Visceral Hypersensitivity Induced By Optogenetic Activation of the Amygdala in Conscious Rats." American Journal of Physiology. Gastrointestinal and Liver Physiology, vol. 314, no. 3, 2018, pp. G448-G457.
Johnson AC, Latorre R, Ligon CO, et al. Visceral hypersensitivity induced by optogenetic activation of the amygdala in conscious rats. Am J Physiol Gastrointest Liver Physiol. 2018;314(3):G448-G457.
Johnson, A. C., Latorre, R., Ligon, C. O., & Greenwood-Van Meerveld, B. (2018). Visceral hypersensitivity induced by optogenetic activation of the amygdala in conscious rats. American Journal of Physiology. Gastrointestinal and Liver Physiology, 314(3), pp. G448-G457. doi:10.1152/ajpgi.00370.2017.
Johnson AC, et al. Visceral Hypersensitivity Induced By Optogenetic Activation of the Amygdala in Conscious Rats. Am J Physiol Gastrointest Liver Physiol. 2018 03 1;314(3):G448-G457. PubMed PMID: 29351398.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Visceral hypersensitivity induced by optogenetic activation of the amygdala in conscious rats. AU - Johnson,Anthony C, AU - Latorre,Rocco, AU - Ligon,Casey O, AU - Greenwood-Van Meerveld,Beverley, Y1 - 2017/12/14/ PY - 2018/1/20/pubmed PY - 2019/2/27/medline PY - 2018/1/20/entrez KW - amygdala KW - bed nucleus of the stria terminalis KW - colon KW - optogenetics KW - pain SP - G448 EP - G457 JF - American journal of physiology. Gastrointestinal and liver physiology JO - Am. J. Physiol. Gastrointest. Liver Physiol. VL - 314 IS - 3 N2 - In vivo optogenetics identifies brain circuits controlling behaviors in conscious animals by using light to alter neuronal function and offers a novel tool to study the brain-gut axis. Using adenoviral-mediated expression, we aimed to investigate whether photoactivation with channelrhodopsin (ChR2) or photoinhibition with halorhodopsin (HR3.0) of fibers originating from the central nucleus of the amygdala (CeA) at the bed nucleus of the stria terminalis (BNST) had any effect on colonic sensitivity. We also investigated whether there was any deleterious effect of the adenovirus on the neuronal population or the neuronal phenotype within the CeA-BNST circuitry activated during the optogenetic stimulation. In male rats, the CeA was infected with vectors expressing ChR2 or HR3.0 and fiber optic cannulae were implanted on the BNST. After 8-10 wk, the response to graded, isobaric colonic distension was measured with and without laser stimulation of CeA fibers at the BNST. Immunohistochemistry and histology were used to evaluate vector expression, neuronal integrity, and neurochemical phenotype. Photoactivation of CeA fibers at the BNST with ChR2 induced colonic hypersensitivity, whereas photoinhibition of CeA fibers at the BNST with HR3.0 had no effect on colonic sensitivity. Control groups treated with virus expressing reporter proteins showed no abnormalities in neuronal morphology, neuronal number, or neurochemical phenotype following laser stimulation. Our experimental findings reveal that optogenetic activation of discrete brain nuclei can be used to advance our understanding of complex visceral nociceptive circuitry in a freely moving rat model. NEW & NOTEWORTHY Our findings reveal that optogenetic technology can be employed as a tool to advance understanding of the brain-gut axis. Using adenoviral-mediated expression of opsins, which were activated by laser light and targeted by fiber optic cannulae, we examined central nociceptive circuits mediating visceral pain in a freely moving rat. Photoactivation of amygdala fibers in the stria terminalis with channelrhodopsin induced colonic hypersensitivity, whereas inhibition of the same fibers with halorhodopsin did not alter colonic sensitivity. SN - 1522-1547 UR - https://www.unboundmedicine.com/medline/citation/29351398/Visceral_hypersensitivity_induced_by_optogenetic_activation_of_the_amygdala_in_conscious_rats_ L2 - http://www.physiology.org/doi/full/10.1152/ajpgi.00370.2017?url_ver=Z39.88-2003&rfr_id=ori:rid:crossref.org&rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -