5-hydroxytryptamine 2C receptors in the dorsal striatum mediate stress-induced interference with negatively reinforced instrumental escape behavior

Strong, P.V.; Christianson, J.P.; Loughridge, A.B.; Amat, J.; Maier, S.F.; Fleshner, M.; Greenwood, B.N.

doi:10.1016/j.neuroscience.2011.09.041

Cited by 61Neurotransmitter Receptor Influence on BehaviorMemory and Neural MechanismsStress Responses and Cortisol

5-hydroxytryptamine 2C receptors in the dorsal striatum mediate stress-induced interference with negatively reinforced instrumental escape behavior

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Strong, P.V., Christianson, J.P., Loughridge, A.B., Amat, J., Maier, S.F., Fleshner, M., Greenwood, B.N.·2011·Neuroscience

DOI 10.1016/j.neuroscience.2011.09.041PMC PMC3235414

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Abstract

Uncontrollable stress can interfere with instrumental learning and induce anxiety in humans and rodents. While evidence supports a role for serotonin (5-HT) and serotonin 2C receptors (5-HT(2C)R) in the behavioral consequences of uncontrollable stress, the specific sites of action are unknown. These experiments sought to delineate the role of 5-HT and 5-HT(2C)R in the dorsal striatum (DS) and the lateral/basolateral amygdala (BLA) in the expression of stress-induced instrumental escape deficits and exaggerated fear, as these structures are critical to instrumental learning and fear behaviors. Using in vivo microdialysis, we first demonstrated that prior uncontrollable, but not controllable, stress sensitizes extracellular 5-HT in the dorsal striatum, a result that parallels prior work in the BLA. Additionally, rats were implanted with bi-lateral cannula in either the DS or the BLA and exposed to uncontrollable tail shock stress. One day later, rats were injected with 5-HT(2C)R antagonist (SB242084) and fear and instrumental learning behaviors were assessed in a shuttle box. Separately, groups of non-stressed rats received an intra-DS or an intra-BLA injection of the 5-HT(2C)R agonist (CP809101) and behavior was observed. Intra-DS injections of the 5-HT(2C)R antagonist prior to fear/escape tests completely blocked the stress-induced interference with instrumental escape learning; a partial block was observed when injections were in the BLA. Antagonist administration in either region did not influence stress-induced fear behavior. In the absence of prior stress, intra-DS administration of the 5-HT(2C)R agonist was sufficient to interfere with escape behavior without enhancing fear, while intra-BLA administration of the 5-HT(2C)R agonist increased fear behavior but had no effect on escape learning. Results reveal a novel role of the 5-HT(2C)R in the DS in the expression of instrumental escape deficits produced by uncontrollable stress and demonstrate that the involvement of 5-HT(2C)R activation in stress-induced behaviors is regionally specific.

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Microinjecting 5-HT2C antagonists into DRN target structures such as the amygdala during later testing blocked the passivity and increased anxiety that normally follow inescapable shock.
“Indeed, microinjection of 5-HT2C antagonists directly into these structures does block the passivity and increased anxiety (Christianson et al., 2010; Strong et al., 2011).”
From Learned helplessness at fifty: Insights from neuroscience. (2016) · cites this paper as Strong et al., 2011
Results §3.4 (page not provided) reports that injecting a 5-HT2C antagonist into the basolateral amygdala before testing partially reduced the escape deficit after uncontrollable stress. It did not reduce exaggerated freezing, the paper’s measure of stress-induced fear. Results §3.2 likewise reports that dorsal-striatum injection improved escape behavior but not exaggerated fear, so this source does not support the claim that the injections blocked both passivity and increased anxiety. (LLM, conf=0.92)
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Deurwaerdère, P. D., Moine, C. L., & Chesselet, M. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.12.006 · Cited by 21 · see citing works

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Learned helplessness at fifty: Insights from neuroscience.
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“Indeed, microinjection of 5-HT2C antagonists directly into these structures does block the passivity and increased anxiety (Christianson et al., 2010; Strong et al., 2011).”
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Female rats are more responsive than are males to the protective effects of voluntary physical activity against the behavioral consequences of inescapable stress
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Swimming improves cognitive reserve in ovariectomized rats and enhances neuroprotection after global cerebral ischemia
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Prior stress interferes with the anxiolytic effect of exercise in c57bl/6j mice.
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Dominance status alters restraint-induced neural activity in brain regions controlling stress vulnerability
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Increased temporal discounting after chronic stress in CHL1-deficient mice is reversed by 5-HT2C agonist Ro 60-0175
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The expression of escape deficits produced by uncontrollable stress are mediated by 5-HT 2C receptors in the dorsal striatum
Strong, P., Loughridge, A. B., Christianson, J. S., Ragole, T., Amat, J., MAIER, S. F., Fleshner, M., & Greenwood, B. (2010) · F1000Research · doi:10.7490/f1000research.696.1
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Extracellular serotonin is enhanced in the striatum, but not in the dorsal hippocampus or prefrontal cortex, in rats subjected to an operant conflict procedure.
Beaufour, C., Bihan, C. L., Hamon, M., & Thiébot, M.-H. (2001) · Behavioral Neuroscience · doi:10.1037/0735-7044.115.1.125 · Cited by 8 · see citing works

Authors: Strong, P. V., Christianson, J. P., Loughridge, A. B., Amat, J., Maier, S. F., Fleshner, M., & Greenwood, B. N.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Greenwood, B.N.
ORCID: Christianson, J.P.
Amat, J.
Maier, S.F.
Fleshner, M.
Greenwood, B.N.
Venue: Neuroscience
Publisher: Elsevier BV
Published: 2011-12
Volume: 197
Pages: 132-144
ISSN: 0306-4522 (ISSN-L)
DOI: 10.1016/j.neuroscience.2011.09.041
PMC: PMC3235414
OpenAlex: W2019756351
Cited by: 61
References: 98
Citations by year: 2025: 2 · 2024: 1 · 2023: 3 · 2022: 1 · 2021: 4 · 2020: 5 · 2019: 6 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 2 · 2014: 7 · 2013: 5 · 2012: 9
FWCI: 2.92
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (NIMH 068283, NIMH 050479, NIMH 082453, NIMH 086665)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords: 5-HT2C receptor, serotonin, dorsal striatum, uncontrollable stress, negative reinforcement, fear behavior, regional specificity, SB242084, microdialysis
MeSH terms: Amygdala, Animals, Behavior, Animal, Conditioning, Operant, Corpus Striatum, Helplessness, Learned, Male, Rats, Inbred F344, Stress, Psychological, Rats, Sprague-Dawley, Microdialysis, Receptor, Serotonin, 5-HT2C, Rats

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5-hydroxytryptamine 2C receptors in the dorsal striatum mediate stress-induced interference with negatively reinforced instrumental escape behavior

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