PAC1 receptor modulation of freezing and flight behavior in periaqueductal gray.
PAC1 receptor
VGAT
darting
early gene expression
fear conditioning
freezing
periaqueductal gray
Journal
Genes, brain, and behavior
ISSN: 1601-183X
Titre abrégé: Genes Brain Behav
Pays: England
ID NLM: 101129617
Informations de publication
Date de publication:
20 Nov 2023
20 Nov 2023
Historique:
revised:
05
11
2023
received:
07
09
2023
accepted:
05
11
2023
medline:
20
11
2023
pubmed:
20
11
2023
entrez:
20
11
2023
Statut:
aheadofprint
Résumé
The midbrain periaqueductal gray (PAG) region is a critical anatomical regulator of fear-related species-specific defensive reactions (SSDRs). Pituitary adenylate-cyclase-activating polypeptide (PACAP), and its main receptor PAC1, play an important role in fear-related behavior and anxiety disorders. However, the function of the PACAP-PAC1 system within the PAG with regards to SSDRs has received little attention. To address this gap, we used transgenic PAC1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12873Subventions
Organisme : NIH HHS
ID : R01-MH115678
Pays : United States
Informations de copyright
© 2023 The Authors. Genes, Brain and Behavior published by International Behavioural and Neural Genetics Society and John Wiley & Sons Ltd.
Références
Fanselow MS, Lester LS. A functional behavioristic approach to aversively motivated behavior: predatory imminence as a determinant of the topography of defensive behavior. In: Bolles RC, Beecher MD, eds. Evolution and Learning. Erlbaum; 1988:185-211.
Perusini JN, Fanselow MS. Neurobehavioral perspectives on the distinction between fear and anxiety. Learn Mem. 2015;22:417-425. doi:10.1101/lm.039180.115
Fanselow MS. Neural organization of the defensive behavior system responsible for fear. Psychon Bull Rev. 1994;1(4):429-438. doi:10.3758/BF03210947
Tovote P, Fadok JP, Lüthi A. Neuronal circuits for fear and anxiety. Nat Rev Neurosci. 2015;16:317-331. doi:10.1038/nrn3945
Brown JS, Kalish HI, Farber IE. Conditioned fear as revealed by magnitude of startle response to an auditory stimulus. J Exp Psychol. 1951;41:317-328. doi:10.1037/h0060166
Trott JM, Hoffman AN, Zhuravka I, Fanselow MS. Conditional and unconditional components of aversively motivated freezing, flight and darting in mice. Elife. 2022;11:e75663. doi:10.7554/eLife.75663
Fanselow MS. The midbrain periaqueductal gray as coordinator of action in response to fear and anxiety. In: Depaulis A, Bandler R, eds. The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Immunohistochemical Organization. Plenum Press; 1991:151-173.
De Oca BM, DeCola JP, Maren S, Fanselow MS. Distinct regions of the periaqueductal gray are involved in the acquisition and expression of defensive responses. J Neurosci. 1998;18:3426-3432. doi:10.1523/jneurosci.18-09-03426.1998
Cameron AA, Khan IA, Westlund KN, Willis WD. The efferent projections of the periaqueductal gray in the rat: a Phaseolus vulgaris-leucoagglutinin study. II. Descending projections. J Comp Neurol. 1995;351:585-601. doi:10.1002/cne.903510408
Floyd NS, Price JL, Ferry AT, Keay KA, Bandler R. Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. J Comp Neurol. 2000;422:556-578. doi:10.1002/1096-9861(20000710)422:4<556::aid-cne6>3.0.co;2-u
Hermann DM, Luppi PH, Peyron C, Hinckel P, Jouvet M. Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars α demonstrated by iontophoretic application of choleratoxin (subunit b). J Chem Neuroanat. 1997;13:1-21. doi:10.1016/s0891-0618(97)00019-7
Kalén P, Karlson M, Wiklund L. Possible excitatory amino acid afferents to nucleus raphe dorsalis of the rat investigated with retrograde wheat germ agglutinin and D-[3H] aspartate tracing. Brain Res. 1985;360:285-297. doi:10.1016/0006-8993(85)91244-2
Newman DB, Hilleary SK, Ginsberg CY. Nuclear terminations of corticoreticular fiber systems in rats. Brain Behav Evol. 1989;34:253-264. doi:10.1159/000116508
Rizvi TA, Ennis M, Behbehani MM, Shipley MT. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: topography and reciprocity. J Comp Neurol. 1991;303:121-131. doi:10.1002/cne.903030111
Deng H, Xiao X, Wang Z. Periaqueductal gray neuronal activities underlie different aspects of defensive behaviors. J Neurosci. 2016;36:7580-7588. doi:10.1523/JNEUROSCI.4425-15.2016
Evans DA, Stempel AV, Vale R, Ruehle S, Lefler Y, Branco T. A synaptic threshold mechanism for computing escape decisions. Nature. 2018;558:590-594. doi:10.1038/s41586-018-0244-6
Wright KM, McDannald MA. Ventrolateral periaqueductal gray neurons prioritize threat probability over fear output. Elife. 2019;8:e45013. doi:10.7554/elife.45013
Hashimoto H, Shintani N, Tanaka K, et al. Altered psychomotor behaviors in mice lacking pituitary adenylate cyclase-activating polypeptide (PACAP). Proc Natl Acad Sci U S A. 2001;98:13355-13360. doi:10.1073/pnas.231094498
Sauvage M, Brabet P, Holsboer F, Bockaert J, Steckler T. Mild deficits in mice lacking pituitary adenylate cyclase-activating polypeptide receptor type 1 (PAC1) performing on memory tasks. Mol Brain Res. 2000;84:79-89. doi:10.1016/s0169-328x(00)00219-9
Otto C, Kovalchuk Y, Wolfer DP, et al. Impairment of mossy fiber long-term potentiation and associative learning in pituitary adenylate cyclase activating polypeptide type I receptor-deficient mice. J Neurosci. 2001;21:5520-5527. doi:10.1523/JNEUROSCI.21-15-05520.2001
Takuma K, Maeda Y, Ago Y, et al. An enriched environment ameliorates memory impairments in PACAP-deficient mice. Behav Brain Res. 2014;272:269-278. doi:10.1016/j.bbr.2014.07.005
Kirry AJ, Herbst MR, Poirier SE, et al. Pituitary adenylate cyclase-activating polypeptide (PACAP) signaling in the prefrontal cortex modulates cued fear learning, but not spatial working memory, in female rats. Neuropharmacology. 2018;133:145-154. doi:10.1016/j.neuropharm.2018.01.010
Rajbhandari AK, Octeau CJ, Gonzalez S, et al. A basomedial amygdala to intercalated cells microcircuit expressing PACAP and its receptor PAC1 regulates contextual fear. J Neurosci. 2021;41:3446-3461. doi:10.1523/JNEUROSCI.2564-20.2021
Meloni EG, Kaye KT, Venkataraman A, Carlezon WA Jr. PACAP increases arc/Arg 3.1 expression within the extended amygdala after fear conditioning in rats. Neurobiol Learn Mem. 2019;157:24-34. doi:10.1016/j.nlm.2018.11.011
Meloni EG, Venkataraman A, Donahue RJ, Carlezon WA Jr. Bi-directional effects of pituitary adenylate cyclase-activating polypeptide (PACAP) on fear-related behavior and c-Fos expression after fear conditioning in rats. Psychoneuroendocrinology. 2016;64:12-21. doi:10.1016/j.psyneuen.2015.11.003
Dore R, Iemolo A, Smith KL, Wang X, Cottone P, Sabino V. CRF mediates the anxiogenic and anti-rewarding, but not the anorectic effects of PACAP. Neuropsychopharmacology. 2013;38:2160-2169. doi:10.1038/npp.2013.113
Gaszner B, Kormos V, Kozicz T, Hashimoto H, Reglodi D, Helyes Z. The behavioral phenotype of pituitary adenylate-cyclase activating polypeptide-deficient mice in anxiety and depression tests is accompanied by blunted c-Fos expression in the bed nucleus of the stria terminalis, central projecting Edinger-Westphal nucleus, ventral lateral septum, and dorsal raphe nucleus. Neuroscience. 2012;202:283-299. doi:10.1016/j.neuroscience.2011.11.046
Hammack SE, Cheung J, Rhodes KM, et al. Chronic stress increases pituitary adenylate cyclase-activating peptide (PACAP) and brain-derived neurotrophic factor (BDNF) mRNA expression in the bed nucleus of the stria terminalis (BNST): roles for PACAP in anxiety-like behavior. Psychoneuroendocrinology. 2009;34:833-843. doi:10.1016/j.psyneuen.2008.12.013
Telegdy G, Adamik A. Neurotransmitter-mediated anxiogenic action of PACAP-38 in rats. Behav Brain Res. 2015;281:333-338. doi:10.1016/j.bbr.2014.12.039
Castorina A, Vogiatzis M, Kang JW, Keay KA. PACAP and VIP expression in the periaqueductal grey of the rat following sciatic nerve constriction injury. Neuropeptides. 2019;74:60-69. doi:10.1016/j.npep.2018.12.002
Hannibal J. Pituitary adenylate cyclase-activating peptide in the rat central nervous system: an immunohistochemical and in situ hybridization study. J Comp Neurol. 2002;453:389-417. doi:10.1002/cne.10418
Joo KM, Chung YH, Kim MK, et al. Distribution of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC1, VPAC2, and PAC1 receptor) in the rat brain. J Comp Neurol. 2004;476:388-413. doi:10.1002/cne.20231
Lee JC, Cho YJ, Kim J, et al. Region-specific changes in the immunoreactivity of vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide receptors (VPAC2, and PAC1 receptor) in the aged rat brains. Brain Res. 2010;1351:32-40. doi:10.1016/j.brainres.2010.06.048
Khodai T, Nunn N, Worth AA, et al. PACAP neurons in the ventromedial hypothalamic nucleus are glucose inhibited and their selective activation induces hyperglycaemia. Front Endocrinol. 2018;9:632. doi:10.3389/fendo.2018.00632
Waschek JA, Baca SM, Akerman S. PACAP and migraine headache: immunomodulation of neural circuits in autonomic ganglia and brain parenchyma. J Headache Pain. 2018;19:1-13. doi:10.1186/s10194-018-0850-6
Condro MC, Matynia A, Foster NN, et al. High-resolution characterization of a PACAP-EGFP transgenic mouse model for mapping PACAP-expressing neurons. J Comp Neurol. 2016;524:3827-3848. doi:10.1002/cne.24035
Fanselow MS, Hoffman AN, Zhuravka I. Timing and the transition between modes in the defensive behavior system. Behav Processes. 2019;166:103890. doi:10.1016/j.beproc.2019.103890
Gruene TM, Flick K, Stefano A, Shea SD, Shansky RM. Sexually divergent expression of active and passive conditioned fear responses in rats. Elife. 2015;4:e11352. doi:10.7554/eLife.11352
Huang LK, Wang MJJ. Image thresholding by minimizing the measures of fuzziness. Pattern Recognit. 1995;28(1):41-51.
Totty MS, Warren N, Huddleston I, et al. Behavioral and brain mechanisms mediating conditioned flight behavior in rats. Sci Rep. 2021;11:8215. doi:10.1038/s41598-021-87559-3
Reichling DB. GABAergic neuronal circuitry in the periaqueductal gray matter. In: Depaulis A, Bandler R, eds. The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Immunohistochemical Organization. Plenum Press; 1991:329-344.
Sandner G, Dessort D, Schmitt P, Karli P. Distribution of GABA in the periaqueductal gray matter. Effects of medial hypothalamic lesions. Brain Res. 1981;224:279-290. doi:10.1016/0006-8993(81)90859-3
Roberto M, Brunelli M. PACAP-38 enhances excitatory synaptic transmission in the rat hippocampal CA1 region. Learn Mem. 2000;7(5):303-311. doi:10.1101/lm.34200
Zhang L, Hernandez VS, Gerfen CR, et al. Behavioral role of PACAP signaling reflects its selective distribution in glutamatergic and GABAergic neuronal subpopulations. Elife. 2021;10:e61718. doi:10.7554/eLife.61718
Liang KC, Melia KR, Miserendino MJ, Falls WA, Campeau S, Davis M. Corticotropin-releasing factor: long-lasting facilitation of the acoustic startle reflex. J Neurosci. 1992;12:2303-2312. doi:10.1523/JNEUROSCI.12-06-02303.1992
Beitz AJ, Shepard RD, Wells WE. The periaqueductal gray-raphe magnus projection contains somatostatin, neurotensin and serotonin but not cholecystokinin. Brain Res. 1983;261:132-137. doi:10.1016/0006-8993(83)91292-1
Li YQ, Jia HG, Rao ZR, Shi JW. Serotonin-, substance P- or leucine-enkephalin-containing neurons in the midbrain periaqueductal gray and nucleus raphe dorsalis send projection fibers to the central amygdaloid nucleus in the rat. Neurosci Lett. 1990;120:124-127. doi:10.1016/0304-3940(90)90184-b
Zeng SL, Li YQ, Rao ZR, Shi JW. Projections from serotonin- and substance P-like immunoreactive neurons in the midbrain periaqueductal gray onto the nucleus reticularis gigantocellularis pars alpha in the rat. Neurosci Lett. 1991;131:205-209. doi:10.1016/0304-3940(91)90614-y
Lovick TA. The periaqueductal gray-rostral medulla connection in the defence reaction: efferent pathways and descending control mechanisms. Behav Brain Res. 1993;58:19-25. doi:10.1016/0166-4328(93)90087-7
Fadok JP, Krabbe S, Markovic M, et al. A competitive inhibitory circuit for selection of active and passive fear responses. Nature. 2017;542:96-100. doi:10.1038/nature21047
Dias BG, Ressler KJ. PACAP and the PAC1 receptor in post-traumatic stress disorder. Neuropsychopharmacology. 2013;38:245-246. doi:10.1038/npp.2012.147
Hoffman AN, Trott JM, Makridis A, Fanselow MS. Anxiety, fear, panic: an approach to assessing the defensive behavior system across the predatory imminence continuum. Learn Behav. 2022;50:339-348. doi:10.3758/s13420-021-00509-x
Fanselow MS. Negative valence systems: sustained threat and the predatory imminence continuum. Emerg Top Life Sci. 2022;6:467-477. doi:10.1042/ETLS20220003