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Molecular mechanisms of group I metabotropic glutamate receptor mediated LTP and LTD in basolateral amygdala in vitro

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Abstract

The roles of group I metabotropic glutamate receptors, metabotropic glutamate receptor 1 (mGluR1) and mGluR5, in regulating synaptic plasticity and metaplasticity in the basolateral amygdala (BLA) remain unclear. The present study examined mGluR1- and mGluR5-mediated synaptic plasticity in the BLA and their respective signaling mechanisms. Bath application of the group I mGluR agonist, 3,5-dihydroxyphenylglycine (DHPG) (20 μM), directly suppressed basal fEPSPs (84.5 ± 6.3% of the baseline). The suppressive effect persisted for at least 30 min after washout; it was abolished by the mGluR1 antagonist 7-(hydroxyimino)cyclopropa[b]chromen-1a-carboxylate ethyl ester (CPCCOEt) but was unaffected by the mGluR5 antagonist 2-methyl-6- (phenylethynyl)-pyridine (MPEP). Interestingly, application of DHPG (at both 2 and 20 μM), regardless of the presence of CPCCOEt, could transform single theta burst stimulation (TBS)-induced short-term synaptic potentiation into a long-term potentiation (LTP). Such a facilitating effect could be blocked by the mGluR5 antagonist MPEP. Blockade of phospholipase C (PLC), the downstream enzyme of group I mGluR, with U73122, prevented both mGluR1- and mGluR5-mediated effects on synaptic plasticity. Nevertheless, blockade of protein kinase C (PKC), the downstream enzyme of PLC, with chelerythrine (5 μM) only prevented the transforming effect of DHPG on TBS-induced LTP and did not affect DHPG-induced long-term depression (LTD). These results suggest that mGluR1 activation induced LTD via a PLC-dependent and PKC-independent mechanism, while the priming action of mGluR5 receptor on the BLA LTP is both PLC and PKC dependent. The BLA metaplasticity mediated by mGluR1 and mGluR5 may provide signal switching mechanisms mediating learning and memory with emotional significance.

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Abbreviations

ACSF:

Artificial cerebrospinal fluid

BLA:

Basolateral amygdala

EC:

External capsule

LTP:

Long-term potentiation

NMDA:

N-methyl-d-aspartate

STP:

Short-term potentiation

TBS:

Theta burst stimulation

±APV:

(±)-2-Amino-5-phosphonovaleric acid

DHPG:

3,5-Dihydroxyphenylglycine

MPEP:

2-Methyl-6-(phenylethynyl)-pyridine

CPCCOEt:

7-(Hydroxyimino)cyclopropa[b]chromen-1a-carboxylate ethyl ester

U73122:

1-[6-[[(17β)-3-Methoxyestra-1,3,5(10)-trien-17-yl]amino]hexyl]-1H-pyrrole-2,5-dione

ACPD:

(1S,3R)-1-aminocyclopentane-1,3-dic

MCPG:

(S)-α-Methyl-4-carboxyphenylglycine

VDCCs:

Voltage-dependent calcium channels

References

  • Abe T, Sugihara H, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1992) Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2+ signal transduction. J Biol Chem 267:13361–13368

    CAS  PubMed  Google Scholar 

  • Abraham PA, Xing G, Zhang L, Yu EZ, Post R, Gamble EH, Li H (2008) beta1- and beta2-adrenoceptor induced synaptic facilitation in rat basolateral amygdala. Brain Res 1209:65–73

    Article  CAS  PubMed  Google Scholar 

  • Aroniadou-Anderjaska V, Post RM, Rogawski MA, Li H (2001) Input-specific LTP and depotentiation in the basolateral amygdala. Neuroreport 12:635–640

    Article  CAS  PubMed  Google Scholar 

  • Awad H, Hubert GW, Smith Y, Levey AI, Conn PJ (2000) Activation of metabotropic glutamate receptor 5 has direct excitatory effects and potentiates NMDA receptor currents in neurons of the subthalamic nucleus. J Neurosci 20:7871–7879

    CAS  PubMed  Google Scholar 

  • Balschun D, Manahan-Vaughan D, Wagner T, Behnisch T, Reymann KG, Wetzel W (1999) A specific role for group I mGluRs in hippocampal LTP and hippocampus-dependent spatial learning. Learn Mem 6:138–152

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving AJ, Seal AJ, Henley JM, Jane DE, Watkins JC, Collingridge GL (1993) Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363:347–350

    Article  CAS  PubMed  Google Scholar 

  • Bortolotto ZA, Bashir ZI, Davies CH, Collingridge GL (1994) A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature 368:740–743

    Article  CAS  PubMed  Google Scholar 

  • Braga MF, Aroniadou-Anderjaska V, Post RM, Li H (2002) Lamotrigine reduces spontaneous and evoked GABAA receptor-mediated synaptic transmission in the basolateral amygdala: implications for its effects in seizure and affective disorders. Neuropharmacology 42:522–529

    Article  CAS  PubMed  Google Scholar 

  • Braga MF, Aroniadou-Anderjaska V, Xie J, Li H (2003) Bidirectional modulation of GABA release by presynaptic glutamate receptor 5 kainate receptors in the basolateral amygdala. J Neurosci 23:442–452

    CAS  PubMed  Google Scholar 

  • Cahill L (1999) A neurobiological perspective on emotionally influenced, long-term memory. Semin Clin Neuropsychiatry 4:266–273

    CAS  PubMed  Google Scholar 

  • Calabresi P, Pisani A, Mercuri NB, Bernardi G (1993) Heterogeneity of metabotropic glutamate receptors in the striatum: electrophysiological evidence. Eur J Neurosci 5:1370–1377

    Article  CAS  PubMed  Google Scholar 

  • Camodeca N, Breakwell NA, Rowan MJ, Anwyl R (1999) Induction of LTD by activation of group I mGluR in the dentate gyrus in vitro. Neuropharmacology 38:1597–1606

    Article  CAS  PubMed  Google Scholar 

  • Capogna M (2014) GABAergic cell type diversity in the basolateral amygdala. Curr Opin Neurobiol 26:110–116

    Article  CAS  PubMed  Google Scholar 

  • Chen A, Hough CJ, Li H (2003) Serotonin type II receptor activation facilitates synaptic plasticity via N-methyl-D-aspartate-mediated mechanism in the rat basolateral amygdala. Neuroscience 119:53–63

    Article  CAS  PubMed  Google Scholar 

  • Chen AQ, Chen XC, Zhou RX, Wang W (2008) Involvement of protein kinase C in NMDAR-dependent long-term potentiation in rat amygdala. Sheng Li Xue Bao 60:737–742

    CAS  PubMed  Google Scholar 

  • Chu Z, Hablitz JJ (1998) Activation of group I mGluRs increases spontaneous IPSC frequency in rat frontal cortex. J Neurophysiol 80:621–627

    CAS  PubMed  Google Scholar 

  • Cohen AS, Raymond CR, Abraham WC (1998) Priming of long-term potentiation induced by activation of metabotropic glutamate receptors coupled to phospholipase C. Hippocampus 8:160–170

    Article  CAS  PubMed  Google Scholar 

  • Davidson RJ, Abercrombie H, Nitschke JB, Putnam K (1999) Regional brain function, emotion and disorders of emotion. Curr Opin Neurobiol 9:228–234

    Article  CAS  PubMed  Google Scholar 

  • Davis M (1998) Are different parts of the extended amygdala involved in fear versus anxiety? Biol Psychiatry 44:1239–1247

    Article  CAS  PubMed  Google Scholar 

  • Doherty AJ, Palmer MJ, Bortolotto ZA, Hargreaves A, Kingston AE, Ornstein PL, Schoepp DD, Lodge D, Collingridge GL (2000) A novel, competitive mGlu(5) receptor antagonist (LY344545) blocks DHPG-induced potentiation of NMDA responses but not the induction of LTP in rat hippocampal slices. Br J Pharmacol 131:239–244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89:4363–4367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Endoh T (2004) Characterization of modulatory effects of postsynaptic metabotropic glutamate receptors on calcium currents in rat nucleus tractus solitarius. Brain Res 1024:212–224

    Article  CAS  PubMed  Google Scholar 

  • Friedl M, Clusmann H, Kral T, Dietrich D, Schramm J (1999) Analysing metabotropic glutamate group III receptor mediated modulation of synaptic transmission in the amygdala-kindled dentate gyrus of the rat. Brain Res 821:117–123

    Article  CAS  PubMed  Google Scholar 

  • Fritsch B, Reis J, Gasior M, Kaminski RM, Rogawski MA (2014) Role of GluK1 kainate receptors in seizures, epileptic discharges, and epileptogenesis. J Neurosci 34:5765–5775

    Article  PubMed  PubMed Central  Google Scholar 

  • Fundytus ME (2001) Glutamate receptors and nociception: implications for the drug treatment of pain. CNS Drugs 15:29–58

    Article  CAS  PubMed  Google Scholar 

  • Huang YY, Kandel ER (1998) Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron 21:169–178

    Article  CAS  PubMed  Google Scholar 

  • Hubert GW, Paquet M, Smith Y (2001) Differential subcellular localization of mGluR1a and mGluR5 in the rat and monkey substantia nigra. J Neurosci 21:1838–1847

    CAS  PubMed  Google Scholar 

  • Jia Z, Lu Y, Henderson J, Taverna F, Romano C, Abramow-Newerly W, Wojtowicz JM, Roder J (1998) Selective abolition of the NMDA component of long-term potentiation in mice lacking mGluR5. Learn Mem 5:331–343

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang X, Chen A, Li H (2005) Histaminergic modulation of excitatory synaptic transmission in the rat basolateral amygdala. Neuroscience 131:691–703

    Article  CAS  PubMed  Google Scholar 

  • Jiang X, Xing G, Yang C, Verma A, Zhang L, Li H (2009) Stress impairs 5-HT2A receptor-mediated serotonergic facilitation of GABA release in juvenile rat basolateral amygdala. Neuropsychopharmacology 34:410–423

    Article  CAS  PubMed  Google Scholar 

  • Kauer JA, Malenka RC, Nicoll RA (1988) NMDA application potentiates synaptic transmission in the hippocampus. Nature 334:250–252

    Article  CAS  PubMed  Google Scholar 

  • Le DC, Holden T, Kullmann DM (2011) Short- and long-term depression at glutamatergic synapses on hippocampal interneurons by group I mGluR activation. Neuropharmacology 60:748–756

    Article  Google Scholar 

  • LeDoux JE (2000) Emotion circuits in the brain. Annu Rev Neurosci 23:155–184

    Article  CAS  PubMed  Google Scholar 

  • Li H, Chen A, Xing G, Wei ML, Rogawski MA (2001) Kainate receptor-mediated heterosynaptic facilitation in the amygdala. Nat Neurosci 4:612–620

    Article  CAS  PubMed  Google Scholar 

  • Li H, Weiss SR, Chuang DM, Post RM, Rogawski MA (1998) Bidirectional synaptic plasticity in the rat basolateral amygdala: characterization of an activity-dependent switch sensitive to the presynaptic metabotropic glutamate receptor antagonist 2S-alpha-ethylglutamic acid. J Neurosci 18:1662–1670

    CAS  PubMed  Google Scholar 

  • Lin HC, Wang SJ, Luo MZ, Gean PW (2000) Activation of group II metabotropic glutamate receptors induces long-term depression of synaptic transmission in the rat amygdala. J Neurosci 20:9017–9024

    CAS  PubMed  Google Scholar 

  • Lu YM, Jia Z, Janus C, Henderson JT, Gerlai R, Wojtowicz JM, Roder JC (1997) Mice lacking metabotropic glutamate receptor 5 show impaired learning and reduced CA1 long-term potentiation (LTP) but normal CA3 LTP. J Neurosci 17:5196–5205

    CAS  PubMed  Google Scholar 

  • Lujan R, Nusser Z, Roberts JD, Shigemoto R, Somogyi P (1996) Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci 8:1488–1500

    Article  CAS  PubMed  Google Scholar 

  • Mannaioni G, Marino MJ, Valenti O, Traynelis SF, Conn PJ (2001) Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21:5925–5934

    CAS  PubMed  Google Scholar 

  • Maren S (1999) Neurotoxic basolateral amygdala lesions impair learning and memory but not the performance of conditional fear in rats. J Neurosci 19:8696–8703

    CAS  PubMed  Google Scholar 

  • Masu M, Nakajima Y, Moriyoshi K, Ishii T, Akazawa C, Nakanashi S (1993) Molecular characterization of NMDA and metabotropic glutamate receptors. Ann N Y Acad Sci 707:153–164

    Article  CAS  PubMed  Google Scholar 

  • McDonald AJ, Beitz AJ, Larson AA, Kuriyama R, Sellitto C, Madl JE (1989) Co-localization of glutamate and tubulin in putative excitatory neurons of the hippocampus and amygdala: an immunohistochemical study using monoclonal antibodies. Neuroscience 30:405–421

    Article  CAS  PubMed  Google Scholar 

  • Miura M, Watanabe M, Offermanns S, Simon MI, Kano M (2002) Group I metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J Neurosci 22:8379–8390

    CAS  PubMed  Google Scholar 

  • Morris SH, Knevett S, Lerner EG, Bindman LJ (1999) Group I mGluR agonist DHPG facilitates the induction of LTP in rat prelimbic cortex in vitro. J Neurophysiol 82:1927–1933

    CAS  PubMed  Google Scholar 

  • Neugebauer V (2001) Peripheral metabotropic glutamate receptors: fight the pain where it hurts. Trends Neurosci 24:550–552

    Article  CAS  PubMed  Google Scholar 

  • Neugebauer V (2002) Metabotropic glutamate receptors—important modulators of nociception and pain behavior. Pain 98:1–8

    Article  CAS  PubMed  Google Scholar 

  • Neugebauer V, Keele NB, Shinnick-Gallagher P (1997) Epileptogenesis in vivo enhances the sensitivity of inhibitory presynaptic metabotropic glutamate receptors in basolateral amygdala neurons in vitro. J Neurosci 17:983–995

    CAS  PubMed  Google Scholar 

  • Neugebauer V, Li W, Bird GC, Bhave G, Gereau RW (2003) Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J Neurosci 23:52–63

    CAS  PubMed  Google Scholar 

  • Otto T, Eichenbaum H, Wiener SI, Wible CG (1991) Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1:181–192

    Article  CAS  PubMed  Google Scholar 

  • Palmer MJ, Irving AJ, Seabrook GR, Jane DE, Collingridge GL (1997) The group I mGlu receptor agonist DHPG induces a novel form of LTD in the CA1 region of the hippocampus. Neuropharmacology 36:1517–1532

    Article  CAS  PubMed  Google Scholar 

  • Pisani A, Calabresi P, Centonze D, Bernardi G (1997) Enhancement of NMDA responses by group I metabotropic glutamate receptor activation in striatal neurones. Br J Pharmacol 120:1007–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pisani A, Gubellini P, Bonsi P, Conquet F, Picconi B, Centonze D, Bernardi G, Calabresi P (2001) Metabotropic glutamate receptor 5 mediates the potentiation of N-methyl-D-aspartate responses in medium spiny striatal neurons. Neuroscience 106:579–587

    Article  CAS  PubMed  Google Scholar 

  • Post RM, Weiss SR, Li H, Smith MA, Zhang LX, Xing G, Osuch EA, McCann UD (1998) Neural plasticity and emotional memory. Dev Psychopathol 10:829–855

    Article  CAS  PubMed  Google Scholar 

  • Potegal M, Hebert M, DeCoster M, Meyerhoff JL (1996) Brief, high-frequency stimulation of the corticomedial amygdala induces a delayed and prolonged increase of aggressiveness in male Syrian golden hamsters. Behav Neurosci 110:401–412

    Article  CAS  PubMed  Google Scholar 

  • Potegal M, Robison S, Anderson F, Jordan C, Shapiro E (2007) Sequence and priming in 15 month-olds’ reactions to brief arm restraint: evidence for a hierarchy of anger responses. Aggress Behav 33:508–518

    Article  PubMed  Google Scholar 

  • Rainnie DG, Mania I, Mascagni F, McDonald AJ (2006) Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala. J Comp Neurol 498:142–161

    Article  PubMed  Google Scholar 

  • Rasia-Filho AA, Londero RG, Achaval M (2000) Functional activities of the amygdala: an overview. J Psychiatry Neurosci 25:14–23

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rogawski MA, Donevan SD (1999) AMPA receptors in epilepsy and as targets for antiepileptic drugs. Adv Neurol 79:947–963

    CAS  PubMed  Google Scholar 

  • Rogawski MA, Gryder D, Castaneda D, Yonekawa W, Banks MK, Lia H (2003) GluR5 kainate receptors, seizures, and the amygdala. Ann N Y Acad Sci 985:150–162

    Article  CAS  PubMed  Google Scholar 

  • Rogawski MA, Kurzman PS, Yamaguchi SI, Li H (2001) Role of AMPA and GluR5 kainate receptors in the development and expression of amygdala kindling in the mouse. Neuropharmacology 40:28–35

    Article  CAS  PubMed  Google Scholar 

  • Saviane C, Savtchenko LP, Raffaelli G, Voronin LL, Cherubini E (2002) Frequency-dependent shift from paired-pulse facilitation to paired-pulse depression at unitary CA3-CA3 synapses in the rat hippocampus. J Physiol 544:469–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt HD, Kimmey BA, Arreola AC, Pierce RC (2015) Group I metabotropic glutamate receptor-mediated activation of PKC gamma in the nucleus accumbens core promotes the reinstatement of cocaine seeking. Addict Biol 20:285–296

    Article  CAS  PubMed  Google Scholar 

  • Schmidt HD, Schassburger RL, Guercio LA, Pierce RC (2013) Stimulation of mGluR5 in the accumbens shell promotes cocaine seeking by activating PKC gamma. J Neurosci 33:14160–14169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schmidt K, Krishnan B, Xia Y, Sun A, Orozco-Cabal L, Pollandt S, Centeno M, Genzer K, Gallagher JP, Shinnick-Gallagher P, Liu J (2011) Cocaine withdrawal reduces group I mGluR-mediated long-term potentiation via decreased GABAergic transmission in the amygdala. Eur J Neurosci 34:177–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Schnabel R, Kilpatrick IC, Collingridge GL (2001) Protein phosphatase inhibitors facilitate DHPG-induced LTD in the CA1 region of the hippocampus. Br J Pharmacol 132:1095–1101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schnabel R, Palmer MJ, Kilpatrick IC, Collingridge GL (1999) A CaMKII inhibitor, KN-62, facilitates DHPG-induced LTD in the CA1 region of the hippocampus. Neuropharmacology 38:605–608

    Article  CAS  PubMed  Google Scholar 

  • Schulz B, Fendt M, Gasparini F, Lingenhohl K, Kuhn R, Koch M (2001) The metabotropic glutamate receptor antagonist 2-methyl-6-(phenylethynyl)-pyridine (MPEP) blocks fear conditioning in rats. Neuropharmacology 41:1–7

    Article  CAS  PubMed  Google Scholar 

  • Selig DK, Lee HK, Bear MF, Malenka RC (1995) Reexamination of the effects of MCPG on hippocampal LTP, LTD, and depotentiation. J Neurophysiol 74:1075–1082

    CAS  PubMed  Google Scholar 

  • Spooren WP, Gasparini F, Bergmann R, Kuhn R (2000a) Effects of the prototypical mGlu(5) receptor antagonist 2-methyl-6-(phenylethynyl)-pyridine on rotarod, locomotor activity and rotational responses in unilateral 6-OHDA-lesioned rats. Eur J Pharmacol 406:403–410

    Article  CAS  PubMed  Google Scholar 

  • Spooren WP, Vassout A, Neijt HC, Kuhn R, Gasparini F, Roux S, Porsolt RD, Gentsch C (2000b) Anxiolytic-like effects of the prototypical metabotropic glutamate receptor 5 antagonist 2-methyl-6-(phenylethynyl)pyridine in rodents. J Pharmacol Exp Ther 295:1267–1275

    CAS  PubMed  Google Scholar 

  • Sung KW, Choi S, Lovinger DM (2001) Activation of group I mGluRs is necessary for induction of long-term depression at striatal synapses. J Neurophysiol 86:2405–2412

    CAS  PubMed  Google Scholar 

  • Thomas MJ, O’Dell TJ (1995) The molecular switch hypothesis fails to explain the inconsistent effects of the metabotropic glutamate receptor antagonist MCPG on long-term potentiation. Brain Res 695:45–52

    Article  CAS  PubMed  Google Scholar 

  • Watabe AM, Carlisle HJ, TJ O’D (2002) Postsynaptic induction and presynaptic expression of group 1 mGluR-dependent LTD in the hippocampal CA1 region. J Neurophysiol 87:1395–1403

    CAS  PubMed  Google Scholar 

  • Wilsch VW, Behnisch T, Jager T, Reymann KG, Balschun D (1998a) When are class I metabotropic glutamate receptors necessary for long-term potentiation? J Neurosci 18:6071–6080

    CAS  PubMed  Google Scholar 

  • Zinebi F, Russell RT, McKernan M, Shinnick-Gallagher P (2001) Comparison of paired-pulse facilitation of AMPA and NMDA synaptic currents in the lateral amygdala. Synapse 42:115–127

    Article  CAS  PubMed  Google Scholar 

  • Zucker RS, Stockbridge N (1983) Presynaptic calcium diffusion and the time courses of transmitter release and synaptic facilitation at the squid giant synapse. J Neurosci 3:1263–1269

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Physiology, Fujian Medical University, Fuzhou, People’s Republic of China

    A. Chen & W. W. Hu

  2. Department of Psychiatry, Uniformed Services University of the Health Sciences, 4301 Jones Bridge Road, Bethesda, MD, 20814-4799, USA

    X. L. Jiang & H. Li

  3. Department of Pediatrics, University of Minnesota, Minneapolis, MN, 55414, USA

    M. Potegal

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  1. A. Chen
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  2. W. W. Hu
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  3. X. L. Jiang
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  5. H. Li
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Correspondence to H. Li.

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Chen, A., Hu, W.W., Jiang, X.L. et al. Molecular mechanisms of group I metabotropic glutamate receptor mediated LTP and LTD in basolateral amygdala in vitro. Psychopharmacology 234, 681–694 (2017). https://doi.org/10.1007/s00213-016-4503-7

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