Volume 8, Issue 2 (Spring 2022)                   Caspian J Neurol Sci 2022, 8(2): 67-75 | Back to browse issues page


XML Print


Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:

Aghighi F, Shabani M, Talaei S A. Morphine Consumption During Lactation Impairs Short-Term Neuronal Plasticity in Rat Offspring CA1 Neurons. Caspian J Neurol Sci 2022; 8 (2) :67-75
URL: http://cjns.gums.ac.ir/article-1-516-en.html
1- Physiology Research Center, Institute for Basic Sciences, Kashan University of Medical Sciences, Kashan, Iran
2- Student Research Committee, Kashan University of Medical Sciences, Kashan, Iran
Full-Text [PDF 1602 kb]   (555 Downloads)     |   Abstract (HTML)  (999 Views)
Full-Text:   (290 Views)
Introduction
Opioids are a group of psychoactive drugs [1]. These substances, such as morphine, codeine, and fentanyl, are common analgesics for reducing post-operative and cancer pain. Still, long-term administration of these drugs is associated with high abuse potential [2]. The result of long-term administration of morphine is changing the functions, structures, and morphology of neural systems [3, 4]. Evidence demonstrates that chronic exposure to morphine reduces neurogenesis and alters synaptic transmission in the adult hippocampus [5]. Synaptic plasticity includes Short-Term Synaptic Plasticity (STP) and Long-Term Synaptic Plasticity (LTP). Paired-Pulse Facilitation (PPF) is synaptic plasticity, i.e., short-term, activity-dependent, and common to most chemically transmitting synapses; it is expressed as an increase in the amplitude of the second of two rapidly Evoked Postsynaptic Excitatory Potentials (EPSPs) [6]. The simplest form of short-term plasticity is manifested in paired-pulse effects, i.e., delivered by consecutive pairs of stimuli; Paired-Pulse Depression (PPD) and Paired-Pulse Facilitation (PPF) [7]. Several studies indicated that chronic exposure to morphine could significantly reduce hippocampal synaptic plasticity and alter normal brain function [8, 9]. For example, Zhou et al. suggested that chronic morphine exposure significantly reduces LTP induction in the CA1 (Cornu Ammonis 1) area of the rat’s hippocampus [10].
In contrast, another study reported that repeated morphine exposure enhanced LTP induction and impaired Long-Term Depression (LTD) induction at the Schaffer’s collaterals to CA1 pathway without affecting the baseline synaptic responses [11]. However, despite considerable growth in our information’s about the impact of chronic morphine exposure on LTP, the effect of this experience on short-term synaptic plasticity in the CA1 area of the rat’s hippocampus remains indefinite. Early postnatal life experiences affect neural circuits’ structure and function and cognitive function [12]. The developing brain is highly susceptible to environmental factors and stressors [13]. Scientists made several efforts to induce cognitive impairment in rodents and primates by administering various neurotoxins responsible for neurodegeneration resulting in memory loss [14]. Ghafari et al. argued that exposure to morphine before and during the gestational and lactation period induces neuronal cell death and changes the hippocampus structure in mice offspring [15]. Our previous study signified that chronic morphine exposure during the lactation period reduces spatial learning and memory and impairs LTP induction in the CA1 area of the rat offspring’s hippocampus [16]. Also, Niu et al. indicated that exposure to morphine during the pregnancy impairs the rat offspring’s spatial memory and synaptic plasticity of dentate gyrus neurons. It seems that reduced GABAergic inhibition plays a role in these effects [17].
Furthermore, studies outlined that Gamma-Aminobutyric Acidergic (GABAergic) synaptic transmission is influenced by morphine [18, 19]. As per evidence, GABAergic inhibition plays an essential role in learning and memory processes [20] and their probable related mechanism, synaptic plasticity [21]. Plenty of GABAergic interneurons is nested in the hippocampus [22]. Maroun and Richter-Levin reported that the GABAergic system had been implicated in short-term hippocampal plasticity [23]. This study aimed to evaluate the effects of morphine exposure during the lactation period on the modulation of short-term synaptic plasticity in the neural circuits of rats’ hippocampal CA1 area.

Materials and Methods
Forty male Wistar rats aged 45 days (120-150 g) were used in this experimental study. The examined rats were housed in a standard animal house at temperature 20-22°C, air humidity 50%-55%, and a 12-12 h light-dark cycle. The animals had access to food and water ad libitum. All experiments were authorized by the Ethical Committee of Kashan University of Medical Sciences, Kashan, Iran, also conducted per the Directive 2010/63/EU on protecting animals used for scientific purposes. The examined animals were divided into one Control group (CO) and 3 groups of rats whose mothers received 5 (M5), 10 (M10), or 20 (M20) mg/kg morphine every 12 hours during the lactation period, subcutaneously. All the rats were deprived of milk on day 21 after the birth. Besides, only two offsprings were picked from each morphine-received mother. Two hours after the last dose of morphine was administered to the mothers, we studied the withdrawal syndrome symptoms in the offspring. The animals were tested by the Intraperitoneal (IP) injection of 2 mg/kg Naloxone hydrochloride (Temad, Iran). Immediately after the injection, rats’ behavior signs were observed for 30 min according to a modified version of the Gellert–Holtzman scale in a Plexiglas chamber (30×30×50 cm). The signs were included the graded (body weight loss during 24 hours after the injection, jumps, abdominal contractions, & wet dog shakes) and the checked signs (irritability, writhing, diarrhea, ptosis, erection, or genital grooming, & teeth chattering) [24]. 

In vivo Electrophysiology
To record field Excitatory Post-Synaptic Potentials (fEPSPs), the rats were anesthetized with urethane (1.5 g/kg, IP) and placed in a stereotaxic apparatus (Borj Sanat, Iran). According to Paxinos and Watson stereotaxic atlas [25], a bipolar stimulating electrode was implanted into the Schaffer’s collaterals (4.2 mm posterior to bregma, 3.8 mm lateral to the midline, & 2.8 mm below the skull), and a monopolar recording electrode was lowered to the CA1 stratum radiatum (3.4 posteriors to bregma, 2.5 mm lateral to the midline, and 2.5 mm below the skull). Electrodes were prepared from Teflon-coated stainless-steel wire (0.008-inch diameter, A-M Systems, USA) exposed only at the tip (tip separation 0.10 mm). The proper location of the electrodes was determined by optimizing the evoked response. Using the eLab system (ScienceBeam, Iran) and related computer software (eProbe), fEPSPs were recorded from the stratum radiatum of the CA1 area of the hippocampus in response to stimulation (two sweeps/min at 30-sec intervals) of the ipsilateral Schaffer’s collaterals. Recording signals were amplified by the eLab amplifier and saved at a 10 kHz sampling rate for offline analysis. Electrical stimulation consisted of constant current rectangular pulses (200 μs, 0.1 Hz, 50–1000 μA) delivered by the eLab isolator. The baseline recording was considered stable when the fEPSP amplitude variation (mV) was less than 10% for at least 20 min. The animals with unstable baseline responses were discarded from the experiments. By increasing the stimulus intensity and measuring the amplitude of the fEPSPs, an Input/Output (I/O) curve was set. The evoked field potentials were measured at five different stimulation intensities, and I/O curves were constructed. The threshold intensity (T) was the lowest intensity that evoked a measurable response. Then, 2T to 5T stimulus intensities were applied. Stimulus intensity was adjusted to provide a response that was 60% of the maximum response as a test pulse. Investigating the Short-Term Synaptic Plasticity (STP), after 30 min stable baseline recording, paired-pulse stimuli were applied at 20, 80, and 200 ms Inter-Stimulus Intervals (ISI).
The collected data were expressed as mean±SEM. Using one-way Analysis of Variance (ANOVA), the Gellert–Holtzman scores of the study groups were analyzed. The averaged waveform of each six fEPSPs was used for statistical analysis. The extent of changes (%) in fEPSPs slope (mV/ms) was normalized concerning the 30 min baseline recording and then was analyzed by ANOVA. Tukey’s test was applied as a post-hoc examination. All statistical analyses were performed in SPSS at P<0.05.

Results
Our results demonstrated that receiving morphine during the lactation period induces the morphine dependence of rats’ offspring, demonstrating withdrawal signs. The overall Gellert-Holtzman score by one-way ANOVA data indicated a significant difference between the study groups (F3,36=14.423; P<0.0001). The overall mean±SEM Gellert-Holtzman score of M5 rats was 10.34±2.76 (Figure 1) and increased to 19.67±5.08 and 22.33±3.68 in M10 and M20 groups, respectively.

According to Tukey’s test data, there was a significant difference between the CO group and the other groups (P<0.001); also between the M5 group and M10 and M20 groups (P<0.01, for both comparisons).
Stimulating Schaffer’s collaterals, evoked responses were recorded from hippocampal CA1 neurons of rats’ offspring. Six sweeps were averaged at each stimulus intensity. The slope of fEPSPs was calculated at 5 different stimulus intensities, and then input-output curves for the study groups were created. One-Way ANOVA results signified a significant difference between the experimental groups in the mean values of stimulus intensity (F3,36=4.036; P<0.001). According to Table 1, the mean stimulus intensity required for evoked responses in the M10 and M20 groups was significantly greater than the CO animals (P<0.01 for both comparisons per set of stimulus intensity).

Furthermore, the statistical analysis of the slope amplitude of fEPSPs in each stimulus intensity demonstrated a significant difference between the evoked responses (F3,36=3.719; P<0.001). As illustrated in Figure 2, receiving morphine during the lactation period caused a significant decrease in the baseline synaptic responses of the offsprings’ CA1 neurons, dose-dependently.

The paired-pulse stimulation paradigm was applied to evaluate the effect of morphine exposure during the lactation period on the excitability of the hippocampal neuronal circuits of rats’ offspring. The one-way ANOVA results outlined a significant difference between the Paired-Pulse Ratio (PPR) of different study groups at 20 and 80 ms Inter-Stimulus Intervals (ISI) (F3,36=7.652; P<0.001 & F3,36=11.839; P<0.001, respectively). There was no significant difference between the PPR of different study groups at 200 ms ISI (Figure 3).

The mean±SEM PPR of the CO animals at 20 ms ISI was 92.44±2.98% and significantly decreased to 77.11±3.48% and 70.76±5.93% in the M10 and M20 groups (P<0.01 for both the comparisons). Tukey’s results also suggested that the PPR of the mean±SEM CO animals at 80 ms ISI was 151.33±8.73% and significantly decreased to 129.38±9.37% and 123.82±12.62% in the M10 and M20 groups (P<0.01 for both the comparisons).

Discussion
We reported that morphine consumption during the lactation period causes morphine dependency in rat offspring. We also demonstrated that besides decreasing the basic synaptic responses, short-term synaptic plasticity of the rats CA1 neurons whose mothers received 10 mg/kg and 20 mg/kg morphine twice daily during the lactation period significantly decreased at 20 and 80 ms ISI. There has often been discussion about whether morphine received by the mother can be detected in breastfed babies or not. According to our information, no investigation on the excretion of morphine in animals’ breast milk was published. Still, Feilberg et al. demonstrated that morphine is detected in human milk only 30 minutes after injection. They also concluded that morphine concentrations are higher in milk than in plasma [26]. Robieux et al. have revealed that 0.8 to 12% of morphine received by the mother can be found in the serum of a breastfed infant [27].
Besides, Tao et al. stated that the intake of morphine during pregnancy and lactation makes 14-day-old rat offspring dependent and reduces the anti-nociceptive morphine effect [28]. At the molecular level, Yang et al. reported that the pre- and post-natal morphine exposure influences the N-Methyl-D-Aspartate (NMDA) receptors-mediated synaptic plasticity in the hippocampus of rat offspring [29]. Our previous study showed that morphine consumption during the lactation period causes morphine dependency, impairs spatial learning and memory, and also decreases synaptic plasticity of hippocampal neural circuits of rat offspring [16]. As a kind of brain disorder, drug dependence alters the function of the neuronal circuit, including altering neuronal plasticity and synaptic transmitter release [30, 31]. Furthermore, the drug’s chronic administration leads to toxicity due to the drug overdose and increased side effects [32]. A study suggested that addiction is an aberrant form of memory associated with synaptic plasticity transformation [33].
Furthermore, morphine dependence affects the plan of a synaptic junction [4, 34]. For example, acute exposure to morphine could alter the strength of present connections that might lead to changes in short-term plasticity [35]. Paired-Pulse stimulation elicited by two similar stimuli is a procedure to study short-term plasticity, i.e., substantial in information processing [36]. Wang et al. found that chronic morphine exposure significantly reduces PPD and frequency depression in rats’ primary visual cortex [35]. These authors previously reported that postsynaptic GABAergic inhibition might be vital for short-term depression in the geniculo-cortical pathway.
Moreover, the GABAergic system is essential for short-term synaptic plasticity [37]. For example, the PPD of field potentials could be induced by normal feedforward or feedback inhibitory influences [38]. The blockade of GABAergic inhibition by GABAA receptors’ antagonists can increase PPR or turn the PPD to PPF [39]. Additionally, variation in presynaptic calcium [7], i.e., responsible for PPF, other mechanisms, such as desensitization of AMPA receptors [40] and GABAergic inhibition [39], are implicated in the organization of PPD. Zhang et al. reported that Glycine receptors affect short-term hippocampal plasticity by influencing GABAA receptors-mediated synaptic currents [37]. As a part of the limbic system, the hippocampus plays an essential role in synaptic plasticity and neural adaptation in the CNS. It has multiple opiate receptors and GABAergic neurons [41]. Central GABAergic neurotransmission has interconnected with the mesolimbic dopaminergic system during addiction processes [42]. It was suggested that μ-opioid receptors connected two GABAergic and opioidergic systems [43]. The result of chronic morphine exposure is the downregulation of ionotropic GABAB receptors in the mice [44]. Morphine treatment has also been shown to decrease GABA release [45], increase GABA uptake, and elevate GABA transporters expression in the hippocampus [46]. Zarrindast et al. reported that GABAergic receptors in the CA1 region of the hippocampus have a vital role in the restoring effect of morphine on the impairment of memory induced by morphine [47]. On the other hand, activating GABAA and GABAB receptors with microinjections of their agonists into the dorsal hippocampus inhibited morphine reward [48, 49]. Therefore, morphine consumption in the hippocampal CA1 neurons of rat offspring can disrupt short-term synaptic plasticity during the lactation period by weakening GABAergic inhibition. 

Conclusion
Morphine exposure during the lactation period has a detrimental impact on the basic synaptic activity and short-term synaptic plasticity of the hippocampal CA1 neuronal circuits of rat offspring.

Ethical Considerations
Compliance with ethical guidelines

All study procedures complied with the ethical standards outlined in the Helsinki Declaration (2013). The Ethical Committee of Kashan University of Medical Sciences, Kashan, Iran approved this study (Code: IR.KAUMS.MEDNT.REC.1396.82).

Funding
This research was supported the Deputy of Research and Technology, Kashan University of Medical Sciences, Kashan (Grant no: 96160). 

Authors contributions
Conceptualization and methodology: All authors; Investigation: Mohammad Shabani; Writing - original draft: Fatemeh Aghighi and Mohammad Shabani; Writing - reviewing & editing, funding acquisition, supervision: Sayyed Alireza Talaei.

Conflict of interest
The authors declared no conflict of interest.

Acknowledgements
The authors thank KAUMS Animal Breeding Center for supplying the animals and Miss Asma Vatankhah for her assistance in data collection.


References
  1. Thakur K, Anand A. Milk metabolites and neurodegeneration: Is there crosstalk? Ann Neurosci. 2015; 22(4):239-43. [DOI:10.5214/ans.0972.7531.220410] [PMID] [PMCID]
  2. Nutt DJ, King LA, Phillips LD. Drug harms in the UK: A multicriteria decision analysis. Lancet. 2010; 376(9752):1558-65. [DOI:10.1016/S0140-6736(10)61462-6]
  3. Motahari AA, Sahraei H, Meftahi GH. Role of nitric oxide on dopamine release and morphine-dependency. Basic Clin Neurosci. 2016; 7(4):283-90. [PMID] [PMCID]
  4. Robinson TE, Kolb B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology. 2004; 47(1):33-46. [DOI:10.1016/j.neuropharm.2004.06.025] [PMID]
  5. Georgoussi ZI, Karoussiotis C, Sotiriou A, Papavranoussi-Daponte D, Polissidis AV, Nikoletopoulou V. The role of κ-Opioid receptor-induced autophagy in synaptic alterations. FASEB J. 2020; 34(S1):1. [DOI:10.1096/fasebj.2020.34.s1.02897]
  6. Santschi LA, Stanton PK. A paired-pulse facilitation analysis of long-term synaptic depression at excitatory synapses in rat hippocampal CA1 and CA3 regions. Brain Res. 2003; 962(1-2):78-91. [DOI:10.1016/S0006-8993(02)03846-5]
  7. Zucker RS. Short-term synaptic plasticity. Annu Rev Neurosci. 1989; 12:13-31. [DOI:10.1146/annurev.ne.12.030189.000305] [PMID]
  8. Elahi-Mahani A, Hosseinmardi N, Janahmadi M, Seyedaghamiri F, Hooshmandi M. The role of CA1 glial cells on augmented LTP in morphine-dependent rats. Paper presented at: Iranian Congress of Physiology and Pharmacology. 11 September 2015; Kashan, Iran. https://www.sid.ir/en/Seminar/ViewPaper.aspx?ID=18620
  9. Pu L, Bao GB, Xu NJ, Ma L, Pei G. Hippocampal long-term potentiation is reduced by chronic opiate treatment and can be restored by re-exposure to opiates. J Neurosci. 2002; 22(5):1914-21. [DOI:10.1523/JNEUROSCI.22-05-01914.2002] [PMID] [PMCID]
  10. Zhou M, Luo P, Lu Y, Li CJ, Wang DS, Lu Q, et al. Imbalance of HCN1 and HCN2 expression in hippocampal CA1 area impairs spatial learning and memory in rats with chronic morphine exposure. Prog Neuropsychopharmacol Biol Psychiatry. 2015; 56:207-14. [DOI:10.1016/j.pnpbp.2014.09.010] [PMID]
  11. Elahi-Mahani A, Heysieattalab S, Hosseinmardi N, Janahmadi M, Seyedaghamiri F, Khoshbouei H. Glial cells modulate hippocampal synaptic plasticity in morphine dependent rats. Brain Res Bull. 2018; 140:97-106. [DOI:10.1016/j.brainresbull.2018.04.006] [PMID]
  12. Morishita H, Hensch TK. Critical period revisited: Impact on vision. Curr Opin Neurobiol. 2008; 18(1):101-7. [DOI:10.1016/j.conb.2008.05.009] [PMID]
  13. Brummelte S, Grunau RE, Chau V, Poskitt KJ, Brant R, Vinall J, et al. Procedural pain and brain development in premature newborns. Ann Neurol. 2012; 71(3):385-96. [DOI:10.1002/ana.22267] [PMID] [PMCID]
  14. Anand A, Banik A, Thakur K, Masters CL. The animal models of dementia and Alzheimer’s disease for pre-clinical testing and clinical translation. Curr Alzheimer Res. 2012; 9(9):1010-29. [DOI:10.2174/156720512803569055] [PMID]
  15. Ghafari S, Golalipour MJ. Prenatal morphine exposure reduces pyramidal neurons in CA1, CA2 and CA3 subfields of mice hippocampus. Iran J Basic Med Sci. 2014; 17(3):155-61. [PMID]
  16. Aghighi F, Mohammadifar M, Banafsheh H, Salami M, Talaei SA. Behavioral and electrophysiological aspects of cognition in neonate rats lactated by morphine addicted mothers. Iran J Basic Med Sci. 2019; 22(9):1059-64. [PMID]
  17. Niu L, Cao B, Zhu H, Mei B, Wang M, Yang Y, et al. Impaired in vivo synaptic plasticity in dentate gyrus and spatial memory in juvenile rats induced by prenatal morphine exposure. Hippocampus. 2009; 19(7):649-57. [DOI:10.1002/hipo.20540] [PMID]
  18. Ghamkharinejad G, Marashi SH, Foolad F, Javan M, Fathollahi Y. Unconditioned and learned morphine tolerance influence hippocampal-dependent short-term memory and the subjacent expression of GABA-A receptor alpha subunits. PloS One. 2021; 16(9):e0253902. [DOI:10.1371/journal.pone.0253902] [PMID] [PMCID]
  19. Ramshini E, Alaei H, Reisi P, Naghdi N, Afrozi H, Alaei S, et al. Effect of intracerebroventricular injection of GABA receptors antagonists on morphine-induced changes in GABA and GLU transmission within the mPFC: An in vivo microdialysis study. Iran J Basic Med Sci. 2019; 22(3):246-50. [PMID]
  20. Bonansco C, Fuenzalida M. Plasticity of hippocampal excitatory-inhibitory balance: Missing the synaptic control in the epileptic brain. Neural Plast. 2016; 2016:8607038. [PMID] [PMCID]
  21. Kim J, Son Y, Kim J, Lee S, Kang S, Park K, et al. Developmental and degenerative modulation of GABAergic transmission in the mouse hippocampus. Int J Dev Neurosci. 2015; 47(Pt B):320-32. [DOI:10.1016/j.ijdevneu.2015.08.009] [PMID]
  22. Somogyi P, Klausberger T. Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol. 2005; 562(Pt 1):9-26. [DOI:10.1113/jphysiol.2004.078915] [PMID] [PMCID]
  23. Chiu CQ, Morse TM, Nani F, Knoflach F, Hernandez MC, Jadi M, et al. Tonic GABAergic activity facilitates dendritic calcium signaling and short-term plasticity. bioRxiv. 2020; 1-17. [DOI:10.1101/2020.04.22.055137]
  24. Miladi-Gorji H, Rashidy-Pour A, Fathollahi Y, Akhavan MM, Semnanian S, Safari M. Voluntary exercise ameliorates cognitive deficits in morphine dependent rats: The role of hippocampal brain-derived neurotrophic factor. Neurobiol Learn Mem. 2011; 96(3):479-91. [DOI:10.1016/j.nlm.2011.08.001] [PMID]
  25. Paxinos G, Watson C. The rat brain in stereotaxic coordinates: Hard cover edition. Amsterdam: Elsevier Science; 2006. https://www.google.com/books/edition/The_Rat_Brain_in_Stereotaxic_Coordinates/0prYfdDbh58C?hl=en&gbpv=0
  26. Feilberg VL, Rosenborg D, Broen Christensen C, Mogensen JV. Excretion of morphine in human breast milk. Acta Anaesthesiol Scand. 1989; 33(5):426-8. [DOI:10.1111/j.1399-6576.1989.tb02938.x] [PMID]
  27. Robieux I, Koren G, Vandenbergh H, Schneiderman J. Morphine excretion in breast milk and resultant exposure of a nursing infant. J Toxicol Clin Toxicol. 1990; 28(3):365-70. [PMID]
  28. Tao PL, Yeh GC, Su CH, Wu YH. Co-administration of dextromethorphan during pregnancy and throughout lactation significantly decreases the adverse effects associated with chronic morphine administration in rat offspring. Life Sci. 2001; 69(20):2439-50. [DOI:10.1016/S0024-3205(01)01316-9]
  29. Yang SN, Yang JM, Wu JN, Kao YH, Hsieh WY, Chao CC, et al. Prenatal exposure to morphine alters kinetic properties of NMDA receptor-mediated synaptic currents in the hippocampus of rat offspring. Hippocampus. 2000; 10(6):654-62. [DOI:10.1002/1098-1063(2000)10:63.0.CO;2-T]
  30. Nestler EJ. Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci. 2001; 2(2):119-28. [DOI:10.1038/35053570] [PMID]
  31. Zhang R, Volkow ND. Brain default-mode network dysfunction in addiction. Neuroimage. 2019; 200:313-31. [DOI:10.1016/j.neuroimage.2019.06.036] [PMID]
  32. Goyal K, Koul V, Singh Y, Anand A. Targeted drug delivery to central nervous system (CNS) for the treatment of neurodegenerative disorders: Trends and advances. Cent Nerv Syst Agents Med Chem. 2014; 14(1):43-59. [DOI:10.2174/1871524914666141030145948] [PMID]
  33. Goldstein RZ, Barrot M, Everitt BJ, Foxe JJ. Addiction in focus: Molecular mechanisms, model systems, circuit maps, risk prediction and the quest for effective interventions. Eur J Neurosci. 2019; 50(3):2007-13. [DOI:10.1111/ejn.14544] [PMID] [PMCID]
  34. Ammon S, Mayer P, Riechert U, Tischmeyer H, Höllt V. Microarray analysis of genes expressed in the frontal cortex of rats chronically treated with morphine and after naloxone precipitated withdrawal. Mol Brain Res. 2003; 112(1-2):113-25. [DOI:10.1016/S0169-328X(03)00057-3]
  35. Wang H, Wei H, Chen B, Zhou Y. Chronic morphine exposure impairs short-term synaptic depression of geniculo-cortical visual pathway in vivo. Neurosci Lett. 2006; 410(3):228-33. [DOI:10.1016/j.neulet.2006.10.005] [PMID]
  36. Markram H, Gupta A, Uziel A, Wang Y, Tsodyks M. Information processing with frequency-dependent synaptic connections. Neurobiol Learn Mem. 1998; 70(1-2):101-12. [DOI:10.1006/nlme.1998.3841] [PMID]
  37. Zhang LH, Xu L, Xu TL. Glycine receptor activation regulates short-term plasticity in CA1 area of hippocampal slices of rats. Biochem Biophys Res Commun. 2006; 344(3):721-6. [DOI:10.1016/j.bbrc.2006.03.198] [PMID]
  38. Sloviter RS. Feedforward and feedback inhibition of hippocampal principal cell activity evoked by perforant path stimulation: GABA-mediated mechanisms that regulate excitability in vivo. Hippocampus. 1991; 1(1):31-40. [DOI:10.1002/hipo.450010105] [PMID]
  39. Rich-Bennett E, Dahl D, Lecompte III B. Modulation of paired-pulse activation in the hippocampal dentate gyrus by cholecystokinin, baclofen and bicuculline. Neuropeptides. 1993; 24(5):263-70. [DOI:10.1016/0143-4179(93)90014-2]
  40. Chen C, Blitz DM, Regehr WG. Contributions of receptor desensitization and saturation to plasticity at the retinogeniculate synapse. Neuron. 2002; 33(5):779-88. [DOI:10.1016/S0896-6273(02)00611-6]
  41. Shi MM, Fan KM, Qiao YN, Xu JH, Qiu LJ, Li X, et al. Hippocampal µ-opioid receptors on GABAergic neurons mediate stress-induced impairment of memory retrieval. Mol Psychiatry. 2020; 25(5):977-92. [DOI:10.1038/s41380-019-0435-z] [PMID] [PMCID]
  42. Johnson SW, North RA. Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci. 1992; 12(2):483-8. [DOI:10.1523/JNEUROSCI.12-02-00483.1992] [PMID] [PMCID]
  43. Xi ZX, Stein EA. GABAergic mechanisms of opiate reinforcement. Alcohol Alcohol. 2002; 37(5):485-94. [PMID]
  44. Narita M, Shibasaki M, Mizuo K, Suzuki T. Changes in G-protein activity mediated through the stimulation of dopamine and GABA B receptors in the mesolimbic dopaminergic system of morphine-sensitized mice. Addict Biol. 2003; 8(3):319-25. [DOI:10.1080/13556210310001602239] [PMID]
  45. Vaughan CW, Ingram SL, Connor MA, Christie MJ. How opioids inhibit GABA-mediated neurotransmission. Nature. 1997; 390(6660):611-4. [DOI:10.1038/37610] [PMID]
  46. Hu JH, Yang N, Ma YH, Zhou XG, Zhang XY, Jiang J, et al. Decrease of morphine-induced reward effects and withdrawal symptoms in mice overexpressing γ-aminobutyric acid transporter I. J Neurosci Res. 2003; 74(4):614-21. [DOI:10.1002/jnr.10780] [PMID]
  47. Zarrindast MR, Hoghooghi V, Rezayof A. Inhibition of morphine-induced amnesia in morphine-sensitized mice: Involvement of dorsal hippocampal GABAergic receptors. Neuropharmacology. 2008; 54(3):569-76. [DOI:10.1016/j.neuropharm.2007.11.004] [PMID]
  48. Zarrindast MR, Massoudi R, Sepehri H, Rezayof A. Involvement of GABAB receptors of the dorsal hippocampus on the acquisition and expression of morphine-induced place preference in rats. Physiol Behav. 2006; 87(1):31-8. [DOI:10.1016/j.physbeh.2005.08.041] [PMID]
  49. Rezayof A, Razavi S, Haeri-Rohani A, Rassouli Y, Zarrindast MR. GABA(A) receptors of hippocampal CA1 regions are involved in the acquisition and expression of morphine-induced place preference. Eur Neuropsychopharmacol. 2007; 17(1):24-31. [DOI:10.1016/j.euroneuro.2006.02.003] [PMID]

 
Type of Study: Research | Subject: Special
Received: 2022/04/6 | Accepted: 2022/04/21 | Published: 2022/04/21

Add your comments about this article : Your username or Email:
CAPTCHA

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

© 2024 CC BY-NC 4.0 | Caspian Journal of Neurological Sciences

Designed & Developed by : Yektaweb