Chronic stress enhances apomorphine-induced stereotyped behavior in mice: Involvement of endogenous opioids

doi:10.1016/0006-8993(84)91156-9

Brain Research

Volume 298, Issue 1, 23 April 1984, Pages 138-140

https://doi.org/10.1016/0006-8993(84)91156-9 Get rights and content

Mice subjected to repeated stressful experiences showed an increase in stereotypic climbing behavior induced by apomorphine thus suggesting a modified sensitivity of dopaminergic receptors. Naltrexone, injected before each stressful experience, reversed this effect of chronic stress indicating an involvement of endogenous opioids.

References (11)

AmirS. et al.
The role of endorphins in stress: evidence and speculations
Neurosci. biobehav. Rev.
(1980)
BroderickP.A. et al.
In vivo electrochemical evidence for an enkephalinergic modulation underlying stereotyped behavior: reversibility by naloxone
Brain Research
(1983)
CostallB. et al.
The mesolimbic system, denervation and the climbing response in the mouse
Europ. J. Pharmacol.
(1980)
De la BaumeS. et al.
Changes in dopamine receptors in mice following morphine treatments
Life Sci.
(1979)
MartresM.P. et al.
Long-term changes in the sensitivity of pre- and postsynaptic dopamine receptors in mouse striatum evidenced by behavioral and biochemical studies
Brain Research
(1977)

There are more references available in the full text version of this article.

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The influence of both acute and chronic restraint stress on the rewarding properties of morphine (1, 2 or 3 mg/kg i.p.) and the aversive effects of naloxone (0.5 mg/kg i.p. ×3 or 1.0 mg/kg i.p.) or bremazocine (0.4 mg/kg i.p.) was investigated. An acute (2 h) but not chronic restraint (2 h daily for 7 days) enhanced the morphine place preference, and elicited a place aversion with a subthreshold dose of bremazocine. This enhancing effect on the reinforcing properties induced by the drugs was prevented by either R(+)-SCH-23390 hydrochloride (R(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H3-benzazepine, 30 μg/kg i.p.) or (±)-sulpiride (60 mg/kg i.p.), 10–20 min prior to the stress session. Naltrexone pretreatment (1 mg/kg i.p.) abolished the stress effect on morphine place preference but not that on bremazocine aversion. Instead, nor-BNI (30 μg/3 μl i.c.v.) abolished the stress's effects on bremazocine aversion, but did not modify those on morphine preference. These results show that: (1) acute stress enhanced the morphine and bremazocine conditioned reinforcing effects meanwhile chronic stress did not modify them; (2) the stimulation of D₁ and D₂ dopamine receptors is necessary for the development of restraint stress-induced sensitization to the conditioned reinforcing effects of drugs; and (3) the stimulation of μ/δ- and κ-opioid receptors seems to be differentially involved.
A model of social stress in dominant mice: Effects on sociosexual behaviour
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The possibility of socially stressing the dominant/aggressive member of a pair of male mice is tested. Male mice (NMRI outbreed strain) were housed in pairs to assess dominant and subordinate roles by agonistic interactions and urine-marking test. Social stress for dominant males consisted in 30 min/day of exposure to their subordinate partner interacting with a female in the adjacent compartment of the cage, for 9 days. Results showed that dominance status was maintained. Behavioural observations indicated that neither the subordinates nor the dominant males habituated to this experimental procedure. At the end of the chronic stress, dominant animals were given the opportunity to interact for 30 min with a female in their compartment. Results indicated that stressed dominants showed impairment in their sexual behaviour and were more oriented towards the physical environment in comparison with control dominants. The behavioural response to apomorphine (0.25 mg/kg) indicated an alteration of the dopaminergic functioning in socially stressed dominant mice. This study suggests that the characteristics of the stressor and the effects of the chronic social stress could be different, according to male social status.
Effect of acute and chronic stress restraint on amphetamine-associated place preference: Involvement of dopamine D<inf>1</inf> and D<inf>2</inf> receptors
1999, European Journal of Pharmacology
The purpose of this study was to determine the d-amphetamine (1.0, 1.5 and 2 mg/kg i.p.)-induced place preference in rats pre-exposed to acute or chronic restraint stress, using the conditioned place preference model. We also studied the involvement of opioid and dopamine mechanisms in the acute restraint stress-induced increase of d-amphetamine-induced place preference. A single restraint session (2 h) but not chronic restraint (2 h/day for 7 days) leading to adaptation to the stressor, enhanced the d-amphetamine-induced place preference. This enhancing effect was prevented by haloperidol administration (0.4 mg/kg i.p.), (±)-sulpiride (60 mg/kg i.p.) or R(+)-SCH-23390 hydrochloride (R(+)-7-chloro-8-hydroxy-3-methyl-1-phenyl-2,3,4,5-tetrahydro-1H-3-benzazepine hydrochloride, 30 μg/kg i.p.) 10–20 min prior to the acute restraint session. However, naltrexone pretreatment (1 or 2 mg/kg i.p.) failed to prevent the acute restraint-induced enhancement of d-amphetamine-induced place preference. These results suggest that: (1) the enhancement of d-amphetamine-induced place preference occurred after a single restraint stress but not following chronic restraint stress, (2) the stimulation of both dopamine D₁ and D₂ receptors is necessary for the development of single restraint stress-induced enhancement of d-amphetamine-induced place preference and (3) apparently, an opioid system is not involved in this acute restraint-induced effect.

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Chronic stress enhances apomorphine-induced stereotyped behavior in mice: Involvement of endogenous opioids

Neurosci. biobehav. Rev.

Brain Research

Europ. J. Pharmacol.

Life Sci.

Brain Research