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The sigma-1 receptor (Sig-1R) chaperone at the endoplasmic reticulum (ER) plays important roles in cellular regulation. Here we found a new function of.
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Thank you for visiting nature. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser or turn off compatibility mode in Internet Explorer. In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript. Neural adaptations in the medial prefrontal cortex mPFC are thought to be crucial in the development and maintenance of addictive behaviors. The present study, using a rat model of behavioral sensitization to cocaine, was designed to determine whether repeated cocaine exposure in vivo is capable of altering 5-HT-induced regulation of glutamatergic transmission in the mPFC. Repeated cocaine administration is not associated with any changes in the levels of 5-HT 2A receptors or regulator of GTP-binding protein signaling 4. These results suggest that cocaine-induced inhibition of 5-HT 2A receptor-mediated enhancement of glutamatergic transmission in the mPFC may be caused, at least in part, by the impairment of coupling of 5-HT 2A receptors with GTP-binding proteins during cocaine withdrawal. These alterations in 5-HT 2A receptor responsiveness in the mPFC may be relevant to the development of behavioral sensitization and withdrawal effects following repeated cocaine administration. Drug-induced long-lasting neural adaptations in the brain reward circuitry are widely proposed to contribute to several core features of addictive behaviors. There is now considerable evidence that neurotransmitter receptors, receptor-mediated signaling, intrinsic neuronal excitability, neuronal morphology, synaptic strength, and gene expression can be substantially altered in response to single or repeated exposure to addictive drugs Nestler, ; Thomas and Malenka, ; Dong et al, ; Hyman et al, Although the mesolimbic dopamine system, consisting of the ventral tegmental area and nucleus accumbens, is considered to be the major brain substrates for the neural adaptations that may underlie drug addiction Hyman et al, ; Kauer and Malenka, , several recent studies have shown that the neuronal excitability and synaptic functions of the medial prefrontal cortex mPFC were also changed during the development of addictive behaviors Wolf, ; Steketee, ; Nasif et al, ; Peterson et al, ; Huang et al, a , b , suggesting that mPFC is critically involved in drug addiction. The mPFC receives a moderate to dense 5-hydroxytryptamine 5-HT innervation originating from raphe nuclei of the midbrain in both primates and rodents Azmitia and Segal, In addition, the raphe nuclei also receive reciprocal glutamatergic projections from the mPFC Sesack et al, In addition to the well-recognized dopaminergic mechanisms in the development of cocaine addiction, an increasing number of evidence indicates that cocaine-induced alterations in 5-HT system in the brain may also contribute to behavioral sequelae of addiction. For example, behavioral studies have shown that withdrawal from intermittent cocaine administration enhances the 5-HT 2A receptor-associated head-shake response Baumann and Rothman, and locomotor activity Filip et al, Furthermore, administration of 5-HT 2A receptor antagonists has been reported to attenuate relapse to cocaine and cocaine-induced reinstatement of cocaine-seeking behavior Fletcher et al, ; Burmeister et al, It is therefore reasonable to speculate that dysregulation of 5-HT 2A receptor function would have a significant role in the development of cocaine addiction. To test this hypothesis, we examine the effect of repeated cocaine administration and withdrawal on the 5-HT 2A receptor-mediated facilitation of glutamatergic transmission in mPFC layer V pyramidal neurons. Here, we provide the first evidence that withdrawal from repeated cocaine administration induces a severe impairment of 5-HT 2A receptor responsiveness to regulate mPFC glutamatergic transmission. During this time, they were handled and weighed daily. All comparisons between saline- and cocaine-treated groups were performed by experimenters blind to group assignment. All efforts were made to minimize the number of animals used and their suffering. Distance traveled was analyzed for estimates of locomotor response. After 2 days of saline injections to habituate the chamber, rats were divided into two groups that received five daily injections of cocaine, DOI, or saline during — hours. Slice preparation and whole-cell patch-clamp recordings were conducted as described previously Huang and Hsu, For whole-cell patch-clamp recording, one slice was transferred to a submerged recording chamber and fixed at the glass bottom of the chamber with a nylon grid on a platinum wire frame. The recording pipettes were pulled from borosilicate capillary tubing and heat-polished. All detected events were re-examined and accepted or rejected based on subjective visual examination. The program then measured amplitudes and intervals between successive detected events. Background current noise was estimated from the baseline with no clear event and was subtracted from signals for analysis. The sEPSCs frequencies were calculated by dividing the total number of detected events by the total time sampled. Events were ranked by amplitude and interevent interval for preparation of cumulative probability distribution. The mPFC slices were homogenized in ice-cold lysis buffer solution catalogue no. L containing a cocktail of protease inhibitors catalogue no. P to avoid protein degradation, and ground with a pellet pestle Kontes glassware, Vineland, NJ. Samples were mixed with cold Optiprep density gradient medium catalogue no. For each experimental group, homogenates from at least three slices were pooled. Only film exposures that were in the linear range of the ECL reaction were used for quantification analysis. Drug doses were selected on the basis of published studies Essman et al, ; Filip et al, ; Wellman et al, ; Dong et al, ; Conductier et al, ; Berg et al, ; Huang et al, a. All drugs used in in vitro experiments were applied by manually switching the superfusate. Drugs were diluted from stock solutions just before application. Other drugs used in this study were dissolved in distilled water. The concentration of DMSO in the perfusion medium was 0. The significance of the difference between the mean was calculated by unpaired Student's t -test. Probability values p of less than 0. Number of animals used is indicated by n. This cocaine regimen is widely used in the literature to induce behavioral sensitization Beurrier and Malenka, ; Dong et al, ; Nasif et al, ; Huang et al, a. The effectiveness of the repeated cocaine treatment on rats was shown by their heightened locomotor activity in response to cocaine challenge injection Figure 1. This enhancing effect persisted through the application of 5-HT and was almost completely reversed after drug washout. Interestingly, the ability of 5-HT to increase the frequency and amplitude of sEPSCs was markedly attenuated in slices from age-matched rats treated with cocaine for 5 days Figure 3a—d. To assess whether changes in 5-HT sensitivity observed in short-term cocaine withdrawal persist after a long-term withdrawal, the effects of repeated cocaine treatment on the ability of 5-HT to increase sEPSC activity were evaluated following 1—14 days of withdrawal. We found that the slices from rats withdrawn from repeated cocaine treatment for 1, 3, 7, or 14 days exhibited comparable impairment of the enhancing effects of 5-HT on the amplitude and frequency of sEPSCs Figure 3f and g. In contrast, no change in the extent of 5-HT-induced enhancement of sEPSCs was observed in slices from rats that were given a single injection of saline or cocaine Supplementary Figure S1. These results suggest that repeated but not single cocaine administration impairs the ability of 5-HT to enhance the spontaneous glutamatergic synaptic activity in mPFC layer V pyramidal neurons and that this effect persists after long-term withdrawal. Behavioral sensitization induced by repeated cocaine administration. Note that cocaine-induced locomotor sensitization was partially prevented by ketanserin pretreatment. The total number of animals examined is shown in parentheses. The data shown in a—c were taken from the same neuron of a rat treated with saline for 5 days followed by a 3-day withdrawal. Repeated cocaine administration decreases 5-hydroxytryptamine 5-HT -induced enhancement of spontaneous excitatory postsynaptic currents sEPSCs in the medial prefrontal cortex mPFC. On the basis of gene sequence and pharmacological profile, 5-HT receptors could be divided into seven families designated 5-HT 1 to 5-HT 7 with at least 14 subtypes Roth, To identify the cellular mechanisms underlying the decreased ability of 5-HT to increase sEPSCs in mPFC layer V pyramidal neurons after cocaine withdrawal, we first pharmacologically examined the subtype of 5-HT receptors responsible for the synaptic potentiation. Dose—response curves in slices from saline- and cocaine-treated rats showed that the maximum effects of 5-HT on the amplitude and frequency of sEPSCs were markedly attenuated by repeated cocaine exposure Figure 5c and d. Together, these results are consistent with the idea that that repeated cocaine exposure may reduce 5-HT 2A receptor signaling at the mPFC excitatory synapses. The maximum effect of 5-hydroxytryptamine 5-HT on spontaneous excitatory postsynaptic currents sEPSCs in the medial prefrontal cortex mPFC is decreased by repeated cocaine administration. The total number of neurons examined is shown in parentheses. A critical question is how the repeated cocaine administration could reduce the 5-HT 2A receptor responsiveness in layer V pyramidal neurons of the mPFC. Considering that cocaine blocks the dopamine reuptake transporter and, thus, acutely increases local dopamine concentrations in brain areas receiving dopaminergic inputs Hyman, , it is therefore possible that activation of dopaminergic receptors in the critical brain areas is required for the aforementioned cocaine-induced decrease of 5-HT 2A receptor function. Because dopaminergic receptors could be divided into two families, D 1 - and D 2 -like receptors Civelli et al, , we administered specific D 1 - or D 2 -like receptor antagonists before cocaine injection. Repeated cocaine administration decreases 5-HT 2A receptor-mediated serotonergic enhancement of spontaneous excitatory postsynaptic currents sEPSCs by the activation of 5-HT 2A receptors. It is known that cocaine also alters 5-HT neurotransmission through blockade of 5-HT transporters and elevation of extracellular levels of 5-HT in reward-related brain regions Bradberry et al, ; Teneud et al, Additional evidence indicated that 5-HT 2 receptors may be involved in the reinforcing properties of cocaine Meert et al, When co-administered with cocaine, ketanserin, but not RS, the 5-HT-induced enhancement of sEPSCs was not impaired in slices from 5-day cocaine-treated rats. In addition, cocaine-induced locomotor sensitization was partially prevented by ketanserin pretreatment Figure 1. However, in contrast to ketanserin, prazosin did not significantly affect the decrease of 5-HT-induced enhancement of sEPSCs in slice from 5-day cocaine-treated rats Figure 6a and b. Together, these findings indicate that the activation of 5-HT 2A receptor is responsible for the inhibitory effect of repeated cocaine administration on 5-HT-induced enhancement of glutamatergic synaptic activity in the mPFC. As reported previously Baumann and Rothman, , intraperitoneal injection of DOI produced significant head-shake and skin-jerk behaviors. Moreover, although repeated DOI administration produced subtle effect on basal locomotor activity, it caused slight but significant suppression of cocaine-induced locomotor sensitivity at the withdrawal time Supplementary Figure S2. We then proceeded to investigate the cellular adaptations triggered by repeated cocaine treatment to alter the responsiveness of 5-HT 2A receptors in the mPFC. One possible mechanism that might account for the cocaine-induced impairment of 5-HT 2A receptor responsiveness is the reduced expression of 5-HT 2A receptors. As shown in Figure 8a , we found no significant difference between cocaine- and saline-treated rats on the levels of 5-HT 2A receptors after 3-day withdrawal. We further explored whether repeated cocaine treatment may alter the membrane distribution of 5-HT 2A receptors using density gradient centrifugation. Immunoblot analysis of gradient fractions showed that most of 5-HT 2A receptors were concentrated at the bottom fractions along with the DRM marker cavelolin The distribution pattern of 5-HT 2A receptors was not significantly changed by repeated cocaine administration and withdrawal when compared with saline-treated control rats Figure 8b. These results suggest that the impaired responsiveness of 5-HT 2A receptors in the mPFC during withdrawal from chronic cocaine administration is not associated with changes in the expression or membrane distribution of 5-HT 2A receptors. Nine fractions were collected from the top and immunoblotted for the indicated proteins. Right, quantitative analysis of the 5-HT 2A receptor distribution was performed by densitometry and calculated in the percentage of the total protein amount in all fractions. RGS proteins consist of four structurally and functionally distinct subfamilies Ross and Wilkie, To explore the possible involvement of RGS4 in the impairment of the 5-HT 2A receptor responsiveness after repeated cocaine administration, we examined the change of RGS4 expression in rats withdrawn from repeated cocaine administration for 3 days. As illustrated in Figure 8c , no detectable changes in the levels of RGS4 were observed in the mPFC from rats treated with cocaine as compared with rats treated with saline. In this study, we provide the first evidence that withdrawal from repeated cocaine treatment in vivo decreases 5-HT 2A receptor-mediated serotonergic enhancement of glutamatergic synaptic activity in layer V pyramidal neurons of the mPFC in vitro. The cellular mechanism mediating this change may result from an increased extracellular concentration of 5-HT on the days of cocaine treatment, which leads to a sustained increase in the activation of 5-HT 2A receptors and thereby decreases the coupling of 5-HT 2A receptors with GTP-binding proteins during the cocaine withdrawal period. We further demonstrate that the levels of 5-HT 2A receptors and RGS4 are not changed during withdrawal from repeated cocaine administration. Cocaine binds with high affinity to the monoamine transporters and blocks the uptake of extracellular dopamine, serotonin, and norepinephrine Hyman, Although adaptive changes in mesolimbic and mesocortical dopaminergic systems are thought to contribute to the development and expression of cocaine-induced behavioral sensitization and addiction, recent findings suggest that alterations in serotonin and norepinephrine systems may also be involved Drouin et al, ; Fletcher et al, ; Burmeister et al, By extending these observations, we show here that withdrawal from repeated cocaine administration reduces 5-HT 2A receptor-mediated serotonergic facilitation of sEPSCs in the mPFC and this effect is likely mediated by the enhanced 5-HT 2A receptor activation in response to repeated cocaine treatment. Two lines of pharmacological evidence support this conclusion. Thus, a persistent decrease observed in 5-HT 2A receptor responsiveness in cocaine-withdrawn mPFC neurons may be attributed to a cocaine-induced increase in extracellular 5-HT concentration in the mPFC to activate specifically 5-HT 2A receptor-dependent signaling cascade during chronic cocaine treatment period. It is noteworthy that a single exposure to cocaine produced no change in the ability of 5-HT 2A receptors to mediate serotonergic enhancement of sEPSCs, indicating marked drug administration paradigm specificity of the cocaine-induced adaptations of the serotonergic systems. Although we found that repeated DOI administration mimics the effects of cocaine to attenuate 5-HT 2A receptor-mediated enhancement of sEPSCs, the time courses of their action are not completely consistent. Repeated cocaine administration suppressed 5-HT 2A receptor function for at least 2 weeks whereas DOI was only effective for 3 days after withdrawal. The reason for this discrepancy is not clear but could be attributable to, at least in part, the different levels of 5-HT 2A receptor signaling activation by repeated cocaine and DOI administration, resulting in stimulating different cellular processes that may vary in their mode of action. However, we could not exclude the possibility that other mechanisms of action, in addition to the control of 5-HT 2A receptor signaling, may contribute to cocaine-induced prolonged reduction of 5-HT 2A receptor responsiveness in the mPFC. Further work is needed to assess this possibility. Interestingly, repeated DOI administration did not elicit cross-sensitization with cocaine but resulted in a reduction of locomotor sensitivity to an acute dose of cocaine Supplementary Figure S2 , supporting the concept that sole stimulation of 5-HT 2A receptors is not sufficient to underlie behavioral sensitization to cocaine. Because antagonism of 5-HT 2A receptors can significantly attenuate the locomotor stimulant effect of cocaine Figure 1 ; McMahon and Cunningham, , the reduction of cocaine-induced locomotor sensitivity following repeated DOI administration may be related to the impairment of 5-HT 2A receptor responsiveness. A leading hypothesis is that activation of postsynaptic 5-HT 2A receptors would elicit the release of an excitatory retrograde messenger, which leads to increased glutamate release from thalamocortical terminals Zhou and Hablitz, ; Lambe and Aghajanian, ; Marek et al, The results of this study support the idea that the increase in sEPSCs in response to 5-HT 2A receptor activation results from the depolarization and excitation of a subpopulation of pyramidal neurons in the deep layers of the mPFC to increase in glutamatergic recurrent network activity and not through activation of the thalamocortical afferents by a retrograde messenger. If activation of postsynaptic 5-HT 2A receptors elicits an increase in sEPSCs by inducing the release of a retrograde messenger, a manipulation of 5-HT 2A G-protein-coupled receptor signaling cascade in the recorded neurons should equally alter the ability of 5-HT 2A receptors to induce an inward current and the release of a retrograde messenger. An intriguing question is as to what mechanism might give rise to cocaine-induced increase in extracellular 5-HT concentration during repeated cocaine administration to regulate 5-HT 2A receptor function and hence to impair persistently the 5-HT-mediated facilitation of sEPSCs during cocaine withdrawal. Multiple mechanisms have been proposed for the desensitization of GTP-binding protein-coupled receptors, including decreasing the coupling of receptors with GTP-binding proteins, increasing receptor internalization from the cell surface, or reducing the total receptor number Gainetdinov et al, Although the molecular mechanisms underlying the desensitization of 5-HT 2A receptors have not yet been clearly established, our results indicate that 5-HT 2A receptor desensitization induced by chronic cocaine administration appears to be due to the reduced ability of 5-HT 2A receptors to couple to GTP-binding proteins, but does not involve receptor downregulation. Additional studies are needed to determine which mechanism may account for the impairment of 5-HT 2A receptor signaling in the mPFC following repeated cocaine administration. The mPFC is known to have an important function in the development of cocaine-induced behavioral sensitization and withdrawal effects Tzschentke, As 5-HT 2A receptors in the mPFC are important for the regulation of moods, this withdrawal-induced deficit of 5-HT 2A receptor function may be clinically relevant with respect to behavioral depression observed after termination of chronic cocaine administration Barr and Markou, This study also provides novel evidence in supporting the view that cocaine withdrawal is associated with desensitization of 5-HT 2A receptor signaling, which may provide a mechanism to fine-tune the effects of 5-HT on glutamatergic synaptic plasticity in the mPFC. Analogous results were also observed in studies examining the synaptic effects following chronic 5-HT 2A receptor agonist administration. However, our findings seemingly conflict with previous reports showing that withdrawal from chronic cocaine treatment enhanced 5-HT 2A receptor-mediated ACTH, prolactin, and corticosterone release in the hypothalamic paraventricular nucleus Levy et al, ; Baumann and Rothman, , ; Carrasco et al, and dopamine release in the nucleus accumbens Yan et al, , suggesting that chronic cocaine administration can produce a withdrawal-induced supersensitivity of 5-HT 2A receptor function. The reason for this discrepancy is unclear but could be attributable to variation among the assay systems used in different brain regions, resulting in stimulating different cellular processes that may vary in their mode of action. We could not exclude the possibility that differences in the basal or cocaine-induced increase in extracellular 5-HT levels among brain regions may also involve in the occurrence of this apparent discrepancy. In conclusion, our data indicate that withdrawal from repeated cocaine treatment in vivo may decrease 5-HT 2A receptor-mediated serotonergic enhancement of glutamatergic synaptic activity in layer V pyramidal neurons of the mPFC. Our data also indicate that cocaine-induced increase in extracellular 5-HT levels may cause profound activation of 5-HT 2A receptor, and thereby desensitize 5-HT 2A receptors. Over the past few years, there has been evidence that enhanced membrane excitability of mPFC pyramidal neurons and excitatory output from the mPFC may contribute to the development of behavioral sensitization to cocaine Pierce et al, ; Kalivas and Duffy, ; Dong et al, ; Nasif et al, The impairment of 5-HT 2A receptor-mediated enhancement of mPFC glutamatergic synaptic transmission after cocaine withdrawal may result in reduced excitability of the intrinsic mPFC circuitry and thus prevent the development of cocaine-induced behavioral sensitization. These findings provide a major advance in establishing correlation and possible link between cocaine-induced neural adaptive changes of 5-HT 2A receptor function in the mPFC and the development of behavioral sensitization and withdrawal effects after chronic cocaine exposure. Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology 36 : — Araneda R, Andrade R Neuroscience 40 : — Azmitia EC, Segal M An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol : — Barr AM, Markou A Psychostimulant withdrawal as an inducing condition in animal models of depression. Neurosci Biobehav Rev 29 : — Chronic cocaine exposure potentiates prolactin and head shake responses to 5-HT2 receptor stimulation in rats. Neuropharmacology 35 : — Alterations in serotonergic responsiveness during cocaine withdrawal in rats: similarities to major depression in humans. 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Brain Res Brain Res Rev 41 : — Systemic and local cocaine increase extracellular serotonin in the nucleus accumbens. Pharmacol Biochem Behav 53 : — Synaptic plasticity in the mesolimbic dopamine system. Tzschentke TM Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog Neurobiol 63 : — Cocaine-induced hypophagia and hyperlocomotion in rats are attenuated by prazosin. Wolf ME The role of excitatory amino acids in behavioral sensitization to psychomotor stimulants. Prog Neurobiol 54 : — Enhanced accumbal dopamine release following 5-HT2A receptor stimulation in rats pretreated with intermittent cocaine. Brain Res : — Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. Download references. We thank Dr TP Su for critical comments on an earlier version of this paper. You can also search for this author in PubMed Google Scholar. The authors declare that there are no actual or potential conflicts of interest. The authors affirm that there are no financial, personal, or other relationships with other people or organizations that have inappropriately influenced or biased the work. Reprints and permissions. Huang, CC. Neuropsychopharmacol 34 , — Download citation. Received : 23 September Revised : 05 January Accepted : 12 January Published : 11 February Issue Date : July Anyone you share the following link with will be able to read this content:. Sorry, a shareable link is not currently available for this article. Provided by the Springer Nature SharedIt content-sharing initiative. Skip to main content Thank you for visiting nature. Download PDF. Abstract Neural adaptations in the medial prefrontal cortex mPFC are thought to be crucial in the development and maintenance of addictive behaviors. Membrane excitability of nucleus accumbens neurons gates the incubation of cocaine craving Article 11 April Effects of muscarinic M 1 receptor stimulation on reinforcing and neurochemical effects of cocaine in rats Article 28 April Role of serotonin neurons in the dorsal raphe nucleus in heroin self-administration and punishment Article Open access 19 September Slice Preparation and Electrophysiology Slice preparation and whole-cell patch-clamp recordings were conducted as described previously Huang and Hsu, Western Blotting For each experimental group, homogenates from at least three slices were pooled. Figure 1. Full size image. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Figure 7. Figure 8. View author publications. Supplementary information. Supplementary Figures PDF kb. Rights and permissions Reprints and permissions. About this article Cite this article Huang, CC. Copy to clipboard. 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