Long-term sensitization of Fos-responsivity in the rat central nervous system after a single stressful experience

Bruijnzeel, Adrie W.; Stam, Rianne; Compaan, J.C.; Croiset, Gerda; Akkermans, L.M.A.; Olivier, Berend; Wiegant, V.M.

doi:10.1016/s0006-8993(98)01350-x

Cited by 70 publications

(27 citation statements)

References 49 publications

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“…Administration of several drugs of abuse results in selective increases in extracellular dopamine levels in the shell of the nucleus accumbens (Pontieri et al, 1995;Nisell et al, 1997;Pierce and Kalivas, 1997a;Tanda et al, 1997;Tanda and Di Chiara, 1998;Barrot et al, 1999;Cadoni and Di Chiara, 1999). In a similar manner, highly palatable foods (Tanda and Di Chiara, 1998;Di Chiara et al, 1999a;Kelley, 1999), mild stress (e.g., foot shock) (Kalivas and Duffy, 1995;Tidey and Miczek, 1997;Bruijnzeel et al, 1999;Wu et al, 1999), and environmental novelty (Rebec et al, 1997;Rebec, 1998) also selectively increase dopamine transmission in the shell of the nucleus accumbens. Our findings are consistent with the hypothesis that the shell and core are functionally distinct, although we found the core, and not the shell, to be responsive to sexual behavior.…”

Section: Sexual Behavior Effects On C-fos Expression In the Shell Andmentioning

confidence: 96%

Sexual Behavior Induction of c-Fos in the Nucleus Accumbens and Amphetamine-Stimulated Locomotor Activity Are Sensitized by Previous Sexual Experience in Female Syrian Hamsters

Bradley¹,

Meisel

2001

J. Neurosci.

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Dopamine transmission in the nucleus accumbens can be activated by drugs, stress, or motivated behaviors, and repeated exposure to these stimuli can sensitize this dopamine response. The objectives of this study were to determine whether female sexual behavior activates nucleus accumbens neurons and whether past sexual experience cross-sensitizes neuronal responses in the nucleus accumbens to amphetamine. Using immunocytochemical labeling, c-Fos expression in different subregions (shell vs core at the rostral, middle, and caudal levels) of the nucleus accumbens was examined in female hamsters that had varying amounts of sexual experience. Female hamsters, given either 6 weeks of sexual experience or remaining sexually naive, were tested for sexual behavior by exposure to adult male hamsters. Previous sexual experience increased c-Fos labeling in the rostral and caudal levels but not in the middle levels of the nucleus accumbens. Testing for sexual behavior increased labeling in the core, but not the shell, of the nucleus accumbens. To validate that female sexual behavior can sensitize neurons in the mesolimbic dopamine pathway, the locomotor responses of sexually experienced and sexually naive females to an amphetamine injection were then compared. Amphetamine increased general locomotor activity in all females. However, sexually experienced animals responded sooner to amphetamine than did sexually naive animals. These data indicate that female sexual behavior can activate neurons in the nucleus accumbens and that sexual experience can cross-sensitize neuronal responses to amphetamine. In addition, these results provide additional evidence for functional differences between the shell and core of the nucleus accumbens and across its anteroposterior axis.Key words: female sexual behavior; nucleus accumbens; shell; core; c-Fos; sensitization; cross-sensitization; amphetamine Dopamine neurons originating in the midbrain ventral tegmental area and projecting to various forebrain nuclei, including the nucleus accumbens, are part of the mesolimbic dopamine system. It has been suggested that this dopamine system is important for the regulation of appetitive behaviors (Mitchell and Gratton, 1994;Salamone, 1994Salamone, , 1996Ikemoto and Panksepp, 1999), as well as self-administration of drugs of abuse (Pierre and Vezina, 1998;Koob, 1999;Lorrain et al., 1999;McKinzie et al., 1999;Peoples et al., 1999;Bradberry et al., 2000). Systemic administration of a variety of drugs of abuse (e.g., cocaine, amphetamine, and heroin) activates dopamine pathways (Pontieri et al., 1995;Nisell et al., 1997;Pierce and Kalivas, 1997a;Tanda et al., 1997;Tanda and Di Chiara, 1998;Barrot et al., 1999;Cadoni and Di Chiara, 1999), and repeated exposure to these pharmacological agents can sensitize these dopamine-responsive neurons (Robinson et al., 1988;Kalivas et al., 1992;Kalivas and Duffy, 1993;Pierce and Kalivas, 1995;Kuczenski et al., 1997;Nisell et al., 1997;Birrell and Balfour, 1998;Heidbreder and Feldon, 1998;Cadoni and Di Chiara, 1999;Ca...

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Section: Sexual Behavior Effects On C-fos Expression In the Shell Andmentioning

confidence: 96%

Sexual Behavior Induction of c-Fos in the Nucleus Accumbens and Amphetamine-Stimulated Locomotor Activity Are Sensitized by Previous Sexual Experience in Female Syrian Hamsters

Bradley¹,

Meisel

2001

J. Neurosci.

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“…For this initial study, we analyzed the frontal cortex because this region has been reported previously to show robust induction of Fos family proteins after stress (Bruijnzeel et al, 1999;Morrow et al, 1999). The brain samples were analyzed by Western blotting using a pan-Fos antibody, which recognizes all known Fos family proteins.…”

Section: Stress Induction Of Fos Family Proteins In Brain: Western Blmentioning

confidence: 99%

Induction of ΔFosB in Reward-Related Brain Structures after Chronic Stress

Perrotti¹,

Hadeishi²,

Ulery³

et al. 2004

J. Neurosci.

295

243

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Acute and chronic stress differentially regulate immediate-early gene (IEG) expression in the brain. Although acute stress induces c-Fos and FosB, repeated exposure to stress desensitizes the c-Fos response, but FosB-like immunoreactivity remains high. Several other treatments differentially regulate IEG expression in a similar manner after acute versus chronic exposure. The form of FosB that persists after these chronic treatments has been identified as ⌬FosB, a splice variant of the fosB gene. This study was designed to determine whether the FosB form induced after chronic stress is also ⌬FosB and to map the brain regions and identify the cell populations that exhibit this effect. Western blotting, using an antibody that recognizes all Fos family members, revealed that acute restraint stress caused robust induction of c-Fos and full-length FosB, as well as a small induction of ⌬FosB, in the frontal cortex (fCTX) and nucleus accumbens (NAc). The induction of c-Fos (and to some extent full-length FosB) was desensitized after 10 d of restraint stress, at which point levels of ⌬FosB were high. A similar pattern was observed after chronic unpredictable stress. By use of immunohistochemistry, we found that chronic restraint stress induced ⌬FosB expression predominantly in the fCTX, NAc, and basolateral amygdala, with lower levels of induction seen elsewhere. These findings establish that chronic stress induces ⌬FosB in several discrete regions of the brain. Such induction could contribute to the long-term effects of stress on the brain.

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“…group, changes in GluR1 mRNA expression were particularly marked in the AI (Figure 4). Changes in the agranular insular and retrosplenial cortex may be related to the emotional state or level of anxiety in the animals since these regions have been shown to be involved in various memory and emotional functions and to be activated by a range of anxiogenic stimuli (Beck and Fibiger, 1995;Yokoyama and Sasaki, 1999;Bruijnzeel et al, 1999;Del Cano et al, 2000;Shibata, 2000). Thus, it is conceivable that alterations in AMPA receptor function may be important in both treatment groups.…”

Section: Cortical Regionsmentioning

confidence: 99%

Differential Effects of Two Chronic Diazepam Treatment Regimes on Withdrawal Anxiety and AMPA Receptor Characteristics

Allison

Pratt

2005

Neuropsychopharmacol

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Withdrawal from chronic benzodiazepines is associated with increased anxiety and seizure susceptibility. Neuroadaptive changes in neural activity occur in limbo-cortical structures although changes at the level of the GABA A receptor do not provide an adequate explanation for these functional changes. We have employed two diazepam treatment regimes known to produce differing effects on withdrawal aversion in the rat and examined whether withdrawal-induced anxiety was accompanied by changes in AMPA receptor characteristics. Rats were given 28 days treatment with diazepam by the intraperitoneal (i.p.) route (5 mg/kg) and the subcutaneous (s.c.) route (15 mg/kg). Withdrawal anxiety in the elevated plus maze was evident in the group withdrawn from chronic s.c. diazepam (relatively more stable plasma levels) but not from the chronic i.p. group (fluctuating daily plasma levels). In the brains of these rats, withdrawal anxiety was accompanied by increased [ 3 H]Ro48 8587 binding in the hippocampus and thalamus, and decreased GluR1 and GluR2 subunit mRNA expression in the amygdala (GluR1 and GluR2) and cortex (GluR1). The pattern of changes was different in the chronic i.p. group where in contrast to the chronic s.c. group, there was reduced [3 H]Ro48 8587 binding in the hippocampus and no alterations in GluR1 and GluR2 subunit expression in the amygdala. While both groups showed reduced GluR1 mRNA subunit expression in the cortex overall, only the agranular insular cortex exhibited marked reductions following chronic i.p. diazepam. Striatal GluR2 mRNA expression was increased in the i.p. group but not the s.c. group. Taken together, these data are consistent with differential neuroadaptive processes in AMPA receptor plasticity being important in withdrawal from chronic benzodiazepines. Moreover, these processes may differ both at a regional and receptor function level according to the behavioral manifestations of withdrawal.

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Long-term sensitization of Fos-responsivity in the rat central nervous system after a single stressful experience

Cited by 70 publications

References 49 publications

Sexual Behavior Induction of c-Fos in the Nucleus Accumbens and Amphetamine-Stimulated Locomotor Activity Are Sensitized by Previous Sexual Experience in Female Syrian Hamsters

Sexual Behavior Induction of c-Fos in the Nucleus Accumbens and Amphetamine-Stimulated Locomotor Activity Are Sensitized by Previous Sexual Experience in Female Syrian Hamsters

Induction of ΔFosB in Reward-Related Brain Structures after Chronic Stress

Differential Effects of Two Chronic Diazepam Treatment Regimes on Withdrawal Anxiety and AMPA Receptor Characteristics

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