Volume 9, Issue 3 (May & June 2018 2018)                   BCN 2018, 9(3): 157-166 | Back to browse issues page


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Taslimi Z, Komaki A, Haghparast A, Sarihi A. Effects of Acute and Chronic Restraint Stress on Reinstatement of Extinguished Methamphetamine-induced Conditioned Place Preference in Rats. BCN. 2018; 9 (3) :157-166
URL: http://bcn.iums.ac.ir/article-1-1046-en.html
1- Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran.
2- Neuroscience Research Center, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran.
3- PhD Neurophysiology Research Center, Hamadan University of Medical Sciences, Hamadan, Iran.
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1. Introduction
Methamphetamine (METH) is a psychostimulant that reinforces behavioral responses and persuades compulsive medicine use and vulnerably to relapse (National Institute on Drug Abuse, 2010). Though the precise neurobiological mechanisms underlying METH addicting behavior remain unknown, while rewarding effect of the drug plays a critical role. In addition, relapse is the most difficult challenge in the treatment of addiction, and its neurobiological mechanisms are still unclear (Sulzer, Sonders, Poulsen, & Galli, 2005). The relationship between stress and drugs has been successfully patterned in rodents and various acute and chronic stressors trigger drug-seeking behavior in them (Conrad et al., 2010; Faravelli et al., 2012). Furthermore, it has been proved that preference for the drug-paired environment can be reinstated by drug priming injections or stressors (Conrad et al., 2010; Sinha, 2008)
Specialized medical researchers have indicated that stress is not only a risk factor in the development of habit but also an urge trigger to drug maltreatment. However, the mechanisms of stress-induced drug relapse are still a matter of debate (De Giovanni, Guzman, Virgolini, & Cancela, 2016). In fact, stressful activities modify the experience of brain areas active in the rewarding effects of psychostimulants (Belujon & Grace, 2011). Also, it has been suggested that environmental stressors produce long-term changes in the function of brain reward pathways in the same way as drugs of abuse do (Quadros & Miczek, 2009)
Exposure to stress increases drug-seeking behavior and the risk of addictive drug  use  in  human  and  animal  models  by the mechanisms  that  are  not  completely  understood  yet (Karimi, Attarzadeh-Yazdi, Yazdi-Ravandi, Hesam, Azizi, Razavi, et al., 2014). Immobilization stress is a kind of psychological stress that produces two major disruptions described in the literary works, decrease in food intake (Marti, Marti, & Armario, 1994) and creation of anxiety (Vyas, Mitra, Shankaranarayana Rao, & Chattarji, 2002; Sotomayor-Zarate et al., 2015). Restraint stress has been used to stimulate reinstatement of extinguished choice in CPP (conditioned  place  preference)  trained animals for different drugs such as METH (Han, Du, Fu, Wang, Song, Wu, et al., 2014), nicotine (Leao, Cruz, & Planeta, 2009) and cocaine (Briand & Blendy, 2013)
Acute stress is sudden and of short duration. This stress results from specific events or situations that involve novelty, unpredictability, a threat to the life, and live with a poor sense of control. While chronic stress is a long-term stuff and unabated stress, resulting from repeated direct exposure to situations that lead to the discharge of stress hormones (Koob, 2008). Stress increases drug-seeking behavior and the risk of addictive drug whose mechanisms are not clearly understood yet. Consequently, in this study, we attempted to examine the effects of acute and chronic restraint stress on the reinstatement of extinguished METH CPP in rats.
2. Methods
2.1. Study animals
The study animals were housed in groups of four in a 12/12 h light/dark cycle (light on between 7:00 AM and 7: 00 PM) with free access to food and water (Parvishan, Taslimi, Ebrahimzadeh, & Haghparast, 2011). Adult male albino Wistar rats (Pasteur Company, Tehran, Iran) weighing 200-280 g were used in these experiments. The animals were randomly assigned to control and treatment plan groups. Each animal was used only once. Rats got familiar with their new environment prior to starting experimental process. All tests were executed according to the guide for the care and use of laboratory animals (National Institutes of Health Newsletter No. 80-23, revised 1996). The study was approved by the Research and Ethics Committee of Hamadan University of Medical Sciences, Hamadan, Iran. 
2.2. Drugs
In  the  present  study,  METH  (Purity ˃98%, donated by the Iran’s Drug Control Headquarters)  dissolved  in  sterile  saline was used.
2.3. Apparatus
2.3.1. Conditioning place preference paradigm 
A  three-compartment  CPP  apparatus  (30  cm×30  cm×40  cm) was  used  in  these  experiments  (Haghparast, Taslimi, Ramin, Azizi, Khodagholi, & Hassanpour-Ezatti, 2011).  Place conditioning was conducted using an un-biased procedure.  The  apparatus  was made  of  Plexiglas which  was  divided  into  three  compartments, two equal size with different  textured  compartments and one smaller size as a null compartment  by  means  of  a  removable  wall, but  distinguishable  by  texture.  To  provide  the  tactile  difference between  the  compartments,  one  of  the  compartments  had  a smooth  floor  while  the  other  compartment  had  a  net-like  floor. Two  preference  compartments  were  differently  striped  black  and white  on  their  walls.  The  null  compartment  was  a  red  tunnel (30  cm×15  cm×40  cm)  connecting  the  two  preference  compartments.  In  this  apparatus,  rats  showed  no  consistent  preference  for either of  large  compartments,  which  supports  our  unbiased  CPP paradigm.  This paradigm took  place  in  five  consecutive  days,  which consisted  of  three  distinct  phases:  preconditioning,  conditioning, and  postconditioning.  In all phases,  the animals  were  tested  during the  same  time  period  each  day. 
Preconditioning phase.  On day 1  (pre-exposure),  each  rat  with  free  access to  all  compartments was placed  separately in  the  apparatus  for  10  minutes .  Animal  displacement  was  recorded  and  analyzed  on  this  day  (pretest  day).  In  the  experimental  setup  used  in this  study,  the  animals  did  not  show  an  unconditioned  preference for  any  compartment.  Animals  were  then  randomly  assigned  to one  of  the  groups  for  place  conditioning  and  6–8  animals  were used  in  each  following  experiment. 
Conditioning phase.  This phase consisted of a 3-day plan of conditioning sessions.  In  this  phase,  the animals  received  two  trials in  which  they  experienced  the  effects  of  the  drugs  while enclosed  to  one  compartment  for  30  min  and other trials  in  which they  experienced  the  effects  of  saline  while  enclosed  in  the  other compartment  by  closing  the  removable wall.  Access to the compartments was blocked on these days. 
Postconditioning phase.  On the fifth day (test day), the removable  wall was  removed,  and  the  rats  could  access  the  entire  apparatus.  The mean time spent  in  compartments  during  a  10-min  period was  recorded  for  each  rat.  In  order  to  calculate  the  conditioning score,  the  difference  in  time  spent  for  the  drug-paired  place  and saline-paired  place (two equal size compartments)  was  measured  as  the  preference  criteria.  Time  spent in  each  compartment  and  animal  displacement  were  recorded  by using  a camera  (Panasonic)  placed  2  m  above  the CPP  boxes  and  locomotion  tracking  was  measured  by  Maze router software (Science Beam company, Iran). A video tracking system for automation of behavioral experiments was used (Ebrahimian, Naghavi, Yazdi, Sadeghzadeh, Taslimi, & Haghparast, 2016).
2.4. Induction of METH extinction
Following  the  preference  test  day,  the  animals  during  the  conditioning  phase  were  exposed  to  extinction  training  with  access  to  all compartments  in  the  CPP  apparatus  without  any  drug  injection  for 30  min  each  day.  This  procedure  was  repeated  for  each  animal  in  the control  and  experimental  groups  until  the  calculated  CPP  scores  in two  consecutive  days  in  extinction  period  became  similar  to  those in  the  preconditioning  day.  Conditioning  score  (CPP  score)  represents  the  time  spent  in  the  drug-paired  place  minus  the  time  spent in  saline-paired  place  which  were  recorded  by  Maze router software. Thus, the  criterion  for  extinction  or  maintenance  of  the  METH rewarding  properties  in  all  groups  was  the  lack  of  significant  differences  in  preference  scores  between  two  consecutive  days  in  the extinction  period  and  the  preference  score  on  the  preconditioning day (Haghparast, Omranifard, Arezoomandan, Ghalandari-Shamami, Taslimi, Vafaei, 2013).
2.5. Restraint Stress Test
To induce acute stress induction, the animals were immobilized for 3 h once a day just before the reinstatement phase.  For chronic stress, the rats  were  exposed  to  immobilization  stress  for  1  h  daily  during  extinction  period in  rodent  immobilization  bags (Santibanez, Gysling, & Forray, 2006; Vyas, Bernal, & Chattarji, 2003). Briefly, each rat was  placed  in  an  acrylic  mesh  restrainer  device  (length  20 cm,  width  7 cm,  height  6 cm)  while  control  rats  were  kept  in  their  home  cages. Immediately after that, all animals were tested for reinstatement of METH-CPP (Quadros & Miczek, 2009).
2.6. Experimental design
2.6.1. METH dose-response effect on conditioned place preference paradigm
In  these  experiments,  a  dose–response  relationship  for  METH on  CPP  paradigm  was  established.  Different doses of  METH  (0.125, 0.25, 0.5, 1, 2  and  4  mg/kg)  were injected  subcutaneously, to CPP induction during  three  days  of  conditioning  phase  (acquisition). In the control group, the animals received saline instead of METH.
2.6.2. Reinstatement of extinguished METH-induced condition place preference in rats
In  this  set  of  experiments,  the animals  were exposed  during  three days  to  one  distinct  chamber  in  the  presence  of  METH (0.5  mg/kg;  SC) and alternative chamber  in  the  presence of  vehicle (Saline). The day after the test  day,  the animals  were given  free  access  to  both  chambers  for  8  days (extinction phase). To  assess  the  METH-induced  reinstatement,  two  groups of  animals  treated  with  ineffective  dose  of  METH  (0.125 and 0.25  mg/kg;  SC),  and  another  group  received  saline  as  a  vehicle  group.  Conditioning  score  and  distance  traveled  were  recorded  during  reinstatement  phase  during a  10-min  period (Figure 1 A, B).
2.6.3. Effect  of  exposure  to  acute restraint  stress  on  reinstatement  of  METH-induced  CPP  in  rats
To  examine  the  possible  role  of   acute application of restraint  stress  on  reinstatement  of  extinguished METH-induced  CPP, animals  passed  conditioning and extinction phase. The day after extinction, the rats were exposed to the restraint stress  for 3-h period, and after 60 min, were placed  in CPP apparatus and received ineffective dose of METH (0.125 mg/kg) to induce reinstatement  phase. Conditioning score and distance traveled were recorded during 10-min period (Figure 1 C).
2.6.4. Effect  of  exposure  to  chronic restraint  stress  on  reinstatement  of  METH-induced  CPP  in  rats
In order to  examine  the  possible  effect of  chronic restraint  stress  in reinstatement  of  extinguished METH-induced CPP, after conditioning phase, the animals received restraint  stress  for 1 h every day. Sixty minutes later, the animals were placed in entire apparatus (free access) to induce extinction phase. The day after extinction phase, the animals received ineffective dose of METH (0.125 mg/kg) to induce reinstatement of METH (Figure 1 D).
2.7. Statistics
Conditioning  score  represents  the  difference  between  the times  spent  in  the  drug-  and  saline-paired  compartments,  and is  expressed  as  mean ± SEM  (standard  error  of  mean).  Data were processed by commercially available software Graph Pad Prism® 5.0.  In  order to compare  the conditioning  scores  and  distance  traveled  obtained  in  all  groups  (vehicle  and  experimental  groups), 1-way  analysis  of  variance  (ANOVA)  and  repeated  measures  or randomized  block  model  followed  by  post  hoc  analysis  (Dunnett’s or  Newman-Keuls  test)  were  used as  appropriated.  P-values less than 0.05 were considered to be statistically significant.
3. Results
In the first set of experiments, we examined the dose response effects of different doses of METH (0.125, 0.25, 0.5, 1, 2 and 4 mg/kg) injected subcutaneously, on CPP paradigm (n=8). One-way ANOVA followed by Dunnett’s test (F6, 55=17.25, P<0.0001) revealed significant differences in conditioning scores among the vehicle (saline) and experimental groups (Figure 2). Our findings showed that the most effective dose of METH is 0.5 mg/kg (P<0.001). 
3.1. Reinstatement of extinguished METH induced CPP in rats
Subcutaneous injection of  METH  (0.5  mg/kg)  during  3  conditioning  days  induced  significant  preference  (P<0.001)  for  the METH-paired  chamber  in  comparison  with  saline-paired  chamber. During the  extinction  period,  without  any  injection,  the  CPP  score was  calculated  every  day.  The  CPP  induction  by  METH  was gradually moderated  over  days  and  the  time  spent  in  METH-paired  chamber did  not  differ  from  the  saline  one  by  the seventh and  eighth  extinction  day.  After the last extinction day, the animals were tested for reinstatement.  Subcutaneous injection of  METH  priming  dose (0.25  mg/kg) could  induce  reinstatement, (F3,23=8.031, P<0.0001) and  CPP  score  on the reinstatement  day  significantly  increased  compared  to  pretest  phase (P<0.001) (Figure 3) (n=8). 
3.2. Effect of exposure to acute restraint stress on reinstatement of METH-induced CPP in rats
In  this  set  of  experiments,  the  possible  effect  of  acute restraint stress  on  reinstatement  of  extinguished  METH-induced  CPP  was  examined. Animals passed conditioning and extinction  phase  as  described  before  but  the  day  after  extinction (reinstatement  phase), animals  were exposed  to restraint stress for 3-h period, (F8,62=6.644, P<0.0001) (Figure 4). Animals  received  ineffective  dose  of  METH  for  reinstatement  (0.125  mg/kg),  after  exposure  to acute restraint stress. Conditioning score and distance traveled were recorded during 10-min period (F2,20=12.27, P=0.0004) (n= 8).  As results shown, ineffective dose of METH for reinstatement induction, together with acute restraint stress could result in METH reinstatement. 
3.3.  Effect of exposure  to chronic restraint  stress  during extinction phase on  the reinstatement  of  METH-induced CPP  in  rats
To assess the chronic stress effects on reinstatement of METH before putting the animals in CPP apparatus, they were exposed to the restraint stress for 1 hour every day during the extinction phase. The CPP score was calculated every day (Figure 1). In this experiment, group chronic stress could diminish extinction phase for one day (F7,63=7.998, P<0.0001) (Figure 5) (n=8). The day after extinction phase, the animals in chronic stress group received ineffective dose of METH for reinstatement (0.125 mg/kg). Comparing the conditioning score between reinstatement day and pretest using student t test showed significant difference (tp[7]=6.271, P<0.001) (Figure 5) indicating that METH ineffective dose for reinstatement induction, together with chronic restraint stress, could result in reinstatement of METH. 
4. Discussion
Stressful situations modify functions in areas of the brain involved in the rewarding effects of psychostimulants. Although all factors responsible for relapse to drug seeking are not completely known, addicting drugs and stress are considered to bring about medication craving and reinstatement of extinguished drug-seeking in retrieving drug abusers (Sadeghzadeh, Babapour, & Haghparast, 2016). The major finding of our study was that the acute and chronic restraint stress potentiates the effect of low-dose METH and could reinstate METH conditioning place preference in the rats. Nevertheless, for the first time, our data provided evidence that chronic immobilization stress could reduce duration of extinction of METH-induced conditioning place preference. Thus the results of the current research further add to the growing literature on the association of stress with urge and reward pathway. 
Drug-associated stimuli, stress, and drugs of abuse are hypothesized to trigger reinstatement to drug reward-related behaviors (Lu, Shepard, Hall, & Shaham, 2003). Previous studies have shown that stressors, such as restraint (Pacchioni, Gioino, Assis, & Cancela, 2002), footshock (Wang, Luo, Ge, Fu, & Han, 2002), butt pinching (Katz & Roth, 1979), and defeat (Covington & Miczek, 2001), efficiently cause drug reward and reinstatement. Interestingly, this current analysis also proves that the duration of restraint stress for causing reinstatement of extinguished METH-CPP. This is despite the fact that acute and chronic stressors have a different and separate efficiency.
It has already been shown that acute restraint stress activates orexin neurons in the lateral hypothalamus, which send projections to the ventral tegmental area, releasing orexins that activate dopaminergic neurons and reward pathway (Tung et al., 2016). Several lines of evidence have also suggested that the reinstatement of drug seeking behaviors is mediated by dopamine receptors (Dai, Kang, Wang, & Ma, 2006; Gilbert et al., 2005). Likewise, Mazid et al. suggested that desperate stress could affect opioid-related learning (Mazid , Hall, Odell, Stafford, Dyer, Van Kempen, et al., 2016). Thus, it confirms that desperate food deprivation facilitate reinstatement of morphine CPP in rats (Sadeghzadeh et al., 2016). Furthermore acute social defeat stress involve on the reinstatement of the CPP caused by cocaine (Montagud-Romero, Aguilar, Maldonado, Manzanedo, Minarro, & Rodriguez-Arias,  2015). 
Conrad et al. reported that cold swim stress can have long-term results on cocaine seeking habit (Conrad et al., 2010). On the other hand, experiments show that chronic stress significantly decreases cocaine-induced activation of reward pathway (Glynn et al., 2016). Also, it has been reported that exposure to chronic stress protocol significantly reduces dopamine extracellular levels induced by cocaine (Sotomayor-Zarate, Abarca, Araya, Renard, Andres, & Gysling, 2015). Past studies have shown that repeated restraint stress with direct exposure enhances excitatory drive to the basolateral amygdala, an area critical for behavioral responses to be anxious (Padival, Quinette, & Rosenkranz, 2013). As we mentioned, chronic stress in our study decreased duration of METH extinction, and animal exposure to reinstatement phase, sooner than those received acute stress or the control group. It seems that chronic stress affects the reward pathway and extinction process since chronic stress may have an aversive impact on daily living, so individuals may tend to cope using drugs. Chronic stress has worst effects than desperate stress. Exposure to stress prevails in all life events and hypothalamic-pituitary-adrenal (HPA) axis dysfunction has been implicated in the development of several psychological disorders that are comorbid with craving (Faravelli et al., 2012)
Mahoney et al. mentioned that stimulant users endorse greater impulsivity, life stress and sensation seeking; however, methamphetamine users endorsed significantly higher number of life stressors and increased life stressors may account for their methamphetamine usage patterns (Mahoney, Thompson-Lake, Cooper, Verrico, Newton, & De La Garza, 2015). Backing the value of environment in drug addiction, our data support the idea that the restraint stress evokes the reinstatement of METH-CPP responses. Together, these studies raise the intriguing opportunity that the behavioral impact of stress exposure on incubation of reinstatement could also be due to alterations in activity within the brain area involved in stress process.  
In summary, acute and chronic restraint stress could reinstate METH CPP by ineffective dose of METH for reinstatement induction. These studies will finally guide us to develop effective ways to cut down craving and prevent urge in abstinent amphetamine abusers. However, further behavioral, electrophysiological and molecular investigations are needed to elucidate brain areas involved in psychological stress and medication relapse.
Ethical Considerations
Compliance with ethical guideline 
Each animal was used only once. Rats got familiar with their new environment prior to starting experimental process. All tests were executed according to the guide for the care and use of laboratory animals (National Institutes of Health Newsletter No. 80-23, revised 1996). The study was approved by the Research and Ethics Committee of Hamadan University of Medical Sciences, Hamadan, Iran.
Funding
This study was supported by the grant No. 940208496 from Hamadan University of Medical Sciences, Hamadan, Iran.
Conflict of interest
The authors declared no conflict of interest.


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  27. Quadros, I. M., & Miczek, K. A. (2009). Two modes of intense cocaine bingeing: increased persistence after social defeat stress and increased rate of intake due to extended access conditions in rats. Psychopharmacology (Berl), 206(1), 109-120. [DOI:10.1007/s00213-009-1584-6]
  28. Sadeghzadeh, F., Babapour, V., & Haghparast, A. (2016). Food deprivation facilitates reinstatement of morphine-induced conditioned place preference: Role of intra-accumbal dopamine D2-like receptors in associating reinstatement of morphine CPP with stress. Synapse. Synapse, 71(4). [DOI:10.1002/syn.21951] [PMID:27902847]
  29. Santibanez, M., Gysling, K., & Forray, M. I. (2006). Desipramine prevents the sustained increase in corticotropin-releasing hormone-like immunoreactivity induced by repeated immobilization stress in the rat central extended amygdala. Journal of Neuroscience Research, 84(6), 1270-1281.  [DOI:10.1002/jnr.21023]
  30. Sinha, R. (2008). Chronic stress, drug use, and vulnerability to addiction. Annals of the New York Academy of Sciences, 1141, 105-130. [DOI:10.1196/annals.1441.030]
  31. Sotomayor-Zarate, R., Abarca, J., Araya, K. A., Renard, G. M., Andres, M. E., & Gysling, K. (2015). Exposure to repeated immobilization stress inhibits cocaine-induced increase in dopamine extracellular levels in the rat ventral tegmental area. Pharmacological Research, 101, 116-123. [DOI:10.1016/j.phrs.2015.08.015]
  32. Sulzer, D., Sonders, M. S., Poulsen, N. W., & Galli, A. (2005). Mechanisms of neurotransmitter release by amphetamines: a review. Progress in Neurobiology, 75(6), 406-433.  [DOI:10.1016/j.pneurobio.2005.04.003]
  33. Tung, L. W., Lu, G. L., Lee, Y. H., Yu, L., Lee, H. J., Leishman, E., Chiou, L. C. (2016). Orexins contribute to restraint stress-induced cocaine relapse by endocannabinoid-mediated disinhibition of dopaminergic neurons. Nature Communications, 7, 12199.  [DOI:10.1038/ncomms12199]
  34. Vyas, A., Bernal, S., & Chattarji, S. (2003). Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Research, 965(1-2), 290-294. [DOI:10.1016/S0006-8993(02)04162-8]
  35. Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons.The Journal of Neuroscience, 22(15), 6810-8. [DOI:10.1523/JNEUROSCI.22-15-06810.2002]
  36. Wang, B., Luo, F., Ge, X. C., Fu, A. H., & Han, J. S. (2002). Effects of lesions of various brain areas on drug priming or footshock-induced reactivation of extinguished conditioned place preference. Brain Research, 950(1-2), 1-9. [DOI:10.1016/S0006-8993(02)02980-3]
Type of Study: Original | Subject: Behavioral Neuroscience
Received: 2017/04/11 | Accepted: 2017/09/15 | Published: 2018/05/1

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31. Sotomayor-Zarate, R., Abarca, J., Araya, K. A., Renard, G. M., Andres, M. E., & Gysling, K. (2015). Exposure to repeated immobilization stress inhibits cocaine-induced increase in dopamine extracellular levels in the rat ventral tegmental area. Pharmacological Research, 101, 116-123. [DOI:10.1016/j.phrs.2015.08.015] [DOI:10.1016/j.phrs.2015.08.015]
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33. Tung, L. W., Lu, G. L., Lee, Y. H., Yu, L., Lee, H. J., Leishman, E., Chiou, L. C. (2016). Orexins contribute to restraint stress-induced cocaine relapse by endocannabinoid-mediated disinhibition of dopaminergic neurons. Nature Communications, 7, 12199. [DOI:10.1038/ncomms12199] [DOI:10.1038/ncomms12199]
34. Vyas, A., Bernal, S., & Chattarji, S. (2003). Effects of chronic stress on dendritic arborization in the central and extended amygdala. Brain Research, 965(1-2), 290-294. [DOI:10.1016/S0006-8993(02)04162-8] [DOI:10.1016/S0006-8993(02)04162-8]
35. Vyas, A., Mitra, R., Shankaranarayana Rao, B. S., & Chattarji, S. (2002). Chronic stress induces contrasting patterns of dendritic remodeling in hippocampal and amygdaloid neurons.The Journal of Neuroscience, 22(15), 6810-8. [DOI:10.1523/JNEUROSCI.22-15-06810.2002] [DOI:10.1523/JNEUROSCI.22-15-06810.2002]
36. Wang, B., Luo, F., Ge, X. C., Fu, A. H., & Han, J. S. (2002). Effects of lesions of various brain areas on drug priming or footshock-induced reactivation of extinguished conditioned place preference. Brain Research, 950(1-2), 1-9. [DOI:10.1016/S0006-8993(02)02980-3] [DOI:10.1016/S0006-8993(02)02980-3]

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