Skip to main content
SpringerLink
Log in

Synaptic Tagging in the ACC: Basic Mechanisms and Functional Implications

  • Chapter
  • First Online:
Synaptic Tagging and Capture

  • 127 Accesses

Abstract

Synaptic tagging and capture (STC) is believed to play important roles in hippocampus-related associative memory. Recent studies in the anterior cingulate cortex (ACC), a key cortical region for pain and emotion, indicate that excitatory synapses are highly plastic and can undergo different forms of plasticity, including long-term potentiation (LTP), long-term depression (LTD), and metaplasticity. STC has been reported in the ACC of adult mice. Considering ACC neurons receive divergent projections from cortical and subcortical areas, STC may provide a key synaptic mechanism for information integration, memory formation, as well as pathological changes in disease conditions. In this chapter, we will first review current knowledge of ACC anatomy and different forms of LTP and LTD in this area. Then, ACC-STC and its functional relevant roles in pain and aging will be reviewed. Due to limited information on synaptic mechanisms, we will explore possible plasticity-related proteins (PRP) as well as diffusible messengers in ACC-STC. Finally, the physiological and pathological significance of ACC-STC will be discussed at the end. Network interaction between ACC and other brain regions, and its synaptic regulation and STC are future directions for basic research.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
eBook
USD 169.00
Price excludes VAT (USA)
Hardcover Book
USD 219.99
Price excludes VAT (USA)

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Alarcon JM, Barco A, Kandel ER (2006) Capture of the late phase of long-term potentiation within and across the apical and basilar dendritic compartments of CA1 pyramidal neurons: synaptic tagging is compartment restricted. J Neurosci 26(1):256–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apkarian AV, Bushnell MC, Treede RD, Zubieta JK (2005) Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9(4):463–484

    Article  PubMed  Google Scholar 

  • Arnow BA, Desmond JE, Banner LL, Glover GH, Solomon A, Polan ML, Lue TF, Atlas SW (2002) Brain activation and sexual arousal in healthy, heterosexual males. Brain 125(Pt 5):1014–1023

    Article  PubMed  Google Scholar 

  • Baltaci SB, Mogulkoc R, Baltaci AK (2019) Molecular mechanisms of early and late LTP. Neurochem Res 44(2):281–296

    Article  CAS  PubMed  Google Scholar 

  • Bartels A, Zeki S (2000) The neural basis of romantic love. Neuroreport 11(17):3829–3834

    Article  CAS  PubMed  Google Scholar 

  • Barthas F, Sellmeijer J, Hugel S, Waltisperger E, Barrot M, Yalcin I (2015) The anterior cingulate cortex is a critical hub for pain-induced depression. Biol Psychiatry 77(3):236–245

    Article  PubMed  Google Scholar 

  • Bissiere S, Plachta N, Hoyer D, McAllister KH, Olpe HR, Grace AA, Cryan JF (2008) The rostral anterior cingulate cortex modulates the efficiency of amygdala-dependent fear learning. Biol Psychiatry 63(9):821–831

    Article  PubMed  Google Scholar 

  • Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361(6407):31–39

    Article  CAS  PubMed  Google Scholar 

  • Bliss TV, Collingridge GL (2013) Expression of NMDA receptor-dependent LTP in the hippocampus: bridging the divide. Mol Brain 6:5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bliss T, Collingridge GL (2019) Persistent memories of long-term potentiation and the N-methyl-d-aspartate receptor. Brain Neurosci Adv 3:2398212819848213

    Article  PubMed  PubMed Central  Google Scholar 

  • Bliss TV, Collingridge GL, Kaang BK, Zhuo M (2016) Synaptic plasticity in the anterior cingulate cortex in acute and chronic pain. Nat Rev Neurosci 17(8):485–496

    Article  CAS  PubMed  Google Scholar 

  • Buchanan SL, Thompson RH, Maxwell BL, Powell DA (1994) Efferent connections of the medial prefrontal cortex in the rabbit. Exp Brain Res 100(3):469–483

    Article  CAS  PubMed  Google Scholar 

  • Bushnell MC, Ceko M, Low LA (2013) Cognitive and emotional control of pain and its disruption in chronic pain. Nat Rev Neurosci 14(7):502–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calejesan AA, Kim SJ, Zhuo M (2000) Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Eur J Pain 4(1):83–96

    Article  CAS  PubMed  Google Scholar 

  • Cassell MD, Wright DJ (1986) Topography of projections from the medial prefrontal cortex to the amygdala in the rat. Brain Res Bull 17(3):321–333

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Koga K, Descalzi G, Qiu S, Wang J, Zhang LS, Zhang ZJ, He XB, Qin X, Xu FQ, Hu J, Wei F, Huganir RL, Li YQ, Zhuo M (2014a) Postsynaptic potentiation of corticospinal projecting neurons in the anterior cingulate cortex after nerve injury. Mol Pain 10:33

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen T, O’Den G, Song Q, Koga K, Zhang MM, Zhuo M (2014b) Adenylyl cyclase subtype 1 is essential for late-phase long term potentiation and spatial propagation of synaptic responses in the anterior cingulate cortex of adult mice. Mol Pain 10:65

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen T, Wang W, Dong YL, Zhang MM, Wang J, Koga K, Liao YH, Li JL, Budisantoso T, Shigemoto R, Itakura M, Huganir RL, Li YQ, Zhuo M (2014c) Postsynaptic insertion of AMPA receptor onto cortical pyramidal neurons in the anterior cingulate cortex after peripheral nerve injury. Mol Brain 7:76

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen T, Taniguchi W, Chen QY, Tozaki-Saitoh H, Song Q, Liu RH, Koga K, Matsuda T, Kaito-Sugimura Y, Wang J, Li ZH, Lu YC, Inoue K, Tsuda M, Li YQ, Nakatsuka T, Zhuo M (2018) Top-down descending facilitation of spinal sensory excitatory transmission from the anterior cingulate cortex. Nat Commun 9(1):1886

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen QY, Li XH, Zhuo M (2021) NMDA receptors and synaptic plasticity in the anterior cingulate cortex. Neuropharmacology 197:108749

    Article  CAS  PubMed  Google Scholar 

  • Chiou CS, Huang CC, Liang YC, Tsai YC, Hsu KS (2012) Impairment of long-term depression in the anterior cingulate cortex of mice with bone cancer pain. Pain 153(10):2097–2108

    Article  PubMed  Google Scholar 

  • Clem RL, Huganir RL (2010) Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330(6007):1108–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coen SJ, Yaguez L, Aziz Q, Mitterschiffthaler MT, Brammer M, Williams SC, Gregory LJ (2009) Negative mood affects brain processing of visceral sensation. Gastroenterology 137(1):253–261, 261 e251–252

    Article  Google Scholar 

  • Craig AD, Reiman EM, Evans A, Bushnell MC (1996) Functional imaging of an illusion of pain. Nature 384(6606):258–260

    Article  CAS  PubMed  Google Scholar 

  • Descalzi G, Li XY, Chen T, Mercaldo V, Koga K, Zhuo M (2012) Rapid synaptic potentiation within the anterior cingulate cortex mediates trace fear learning. Mol Brain 5:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devinsky O, Morrell MJ, Vogt BA (1995) Contributions of anterior cingulate cortex to behaviour. Brain 118(Pt 1):279–306

    Article  PubMed  Google Scholar 

  • Ding Y, Wang Y, Cao L (2021) A simplified plasticity model based on synaptic tagging and capture theory: simplified STC. Front Comput Neurosci 15:798418

    Article  PubMed  Google Scholar 

  • Eisenberger NI, Lieberman MD, Williams KD (2003) Does rejection hurt? An FMRI study of social exclusion. Science 302(5643):290–292

    Article  CAS  PubMed  Google Scholar 

  • Foland-Ross LC, Gilbert BL, Joormann J, Gotlib IH (2015) Neural markers of familial risk for depression: an investigation of cortical thickness abnormalities in healthy adolescent daughters of mothers with recurrent depression. J Abnorm Psychol 124(3):476–485

    Article  PubMed  PubMed Central  Google Scholar 

  • Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304(5672):881–883

    Article  CAS  PubMed  Google Scholar 

  • Frey U, Morris RG (1998a) Synaptic tagging: implications for late maintenance of hippocampal long-term potentiation. Trends Neurosci 21(5):181–188

    Article  CAS  PubMed  Google Scholar 

  • Frey U, Morris RG (1998b) Weak before strong: dissociating synaptic tagging and plasticity-factor accounts of late-LTP. Neuropharmacology 37(4–5):545–552

    Article  CAS  PubMed  Google Scholar 

  • Gabbott PL, Warner TA, Jays PR, Salway P, Busby SJ (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 492(2):145–177

    Article  PubMed  Google Scholar 

  • Gross C, Hen R (2004) The developmental origins of anxiety. Nat Rev Neurosci 5(7):545–552

    Article  CAS  PubMed  Google Scholar 

  • Grover LM (1998) Evidence for postsynaptic induction and expression of NMDA receptor independent LTP. J Neurophysiol 79(3):1167–1182

    Article  CAS  PubMed  Google Scholar 

  • Hubbard CS, Khan SA, Xu S, Cha M, Masri R, Seminowicz DA (2015) Behavioral, metabolic and functional brain changes in a rat model of chronic neuropathic pain: a longitudinal MRI study. NeuroImage 107:333–344

    Article  PubMed  Google Scholar 

  • Jeon D, Kim S, Chetana M, Jo D, Ruley HE, Lin SY, Rabah D, Kinet JP, Shin HS (2010) Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC. Nat Neurosci 13(4):482–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johansen JP, Fields HL (2004) Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal. Nat Neurosci 7(4):398–403

    Article  CAS  PubMed  Google Scholar 

  • Junho CVC, Caio-Silva W, Trentin-Sonoda M, Carneiro-Ramos MS (2020) An overview of the role of calcium/calmodulin-dependent protein kinase in cardiorenal syndrome. Front Physiol 11:735

    Article  PubMed  PubMed Central  Google Scholar 

  • Kain ZN, Mayes LC, Caldwell-Andrews AA, Karas DE, McClain BC (2006) Preoperative anxiety, postoperative pain, and behavioral recovery in young children undergoing surgery. Pediatrics 118(2):651–658

    Article  PubMed  Google Scholar 

  • Kang SJ, Liu MG, Chen T, Ko HG, Baek GC, Lee HR, Lee K, Collingridge GL, Kaang BK, Zhuo M (2012) Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. J Neurosci 32(33):11318–11329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelly L, Farrant M, Cull-Candy SG (2009) Synaptic mGluR activation drives plasticity of calcium-permeable AMPA receptors. Nat Neurosci 12(5):593–601. https://doi.org/10.1038/nn.2309

  • Kim SS, Wang H, Li XY, Chen T, Mercaldo V, Descalzi G, Wu LJ, Zhuo M (2011) Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice. Mol Brain 4:6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ko HG, Choi JH, Park DI, Kang SJ, Lim CS, Sim SE, Shim J, Kim JI, Kim S, Choi TH, Ye S, Lee J, Park P, Kim S, Do J, Park J, Islam MA, Kim HJ, Turck CW, Collingridge GL, Zhuo M, Kaang BK (2018a) Rapid turnover of cortical NCAM1 regulates synaptic reorganization after peripheral nerve injury. Cell Rep 22(3):748–759

    Article  CAS  PubMed  Google Scholar 

  • Ko HG, Ye S, Han DH, Park P, Lim CS, Lee K, Zhuo M, Kaang BK (2018b) Transcription-independent expression of PKMzeta in the anterior cingulate cortex contributes to chronically maintained neuropathic pain. Mol Pain 14:1744806918783943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koga K, Descalzi G, Chen T, Ko HG, Lu J, Li S, Son J, Kim T, Kwak C, Huganir RL, Zhao MG, Kaang BK, Collingridge GL, Zhuo M (2015) Coexistence of two forms of LTP in ACC provides a synaptic mechanism for the interactions between anxiety and chronic pain. Neuron 86(4):1109

    Article  CAS  PubMed  Google Scholar 

  • Koga K, Li S, Zhuo M (2016) Metabotropic glutamate receptor dependent cortical plasticity in chronic pain. Curr Neuropharmacol 14(5):427–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koga K, Yao I, Setou M, Zhuo M (2017) SCRAPPER selectively contributes to spontaneous release and presynaptic long-term potentiation in the anterior cingulate cortex. J Neurosci 37(14):3887–3895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Leknes S, Tracey I (2008) A common neurobiology for pain and pleasure. Nat Rev Neurosci 9(4):314–320

    Article  CAS  PubMed  Google Scholar 

  • Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M (2010) Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 330(6009):1400–1404

    Article  CAS  PubMed  Google Scholar 

  • Li XH, Song Q, Chen T, Zhuo M (2017) Characterization of postsynaptic calcium signals in the pyramidal neurons of anterior cingulate cortex. Mol Pain 13:1744806917719847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XH, Matsuura T, Liu RH, Xue M, Zhuo M (2019) Calcitonin gene-related peptide potentiated the excitatory transmission and network propagation in the anterior cingulate cortex of adult mice. Mol Pain 15:1744806919832718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li XH, Matsuura T, Xue M, Chen QY, Liu RH, Lu JS, Shi W, Fan K, Zhou Z, Miao Z, Yang J, Wei S, Wei F, Chen T, Zhuo M (2021) Oxytocin in the anterior cingulate cortex attenuates neuropathic pain and emotional anxiety by inhibiting presynaptic long-term potentiation. Cell Rep 36(3):109411

    Article  CAS  PubMed  Google Scholar 

  • Liauw J, Wang GD, Zhuo M (2003) NMDA receptors contribute to synaptic transmission in anterior cingulate cortex of adult mice. Sheng Li Xue Bao 55(4):373–380

    CAS  PubMed  Google Scholar 

  • Liauw J, Wu LJ, Zhuo M (2005) Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex. J Neurophysiol 94(1):878–882

    Article  CAS  PubMed  Google Scholar 

  • Liu MG, Kang SJ, Shi TY, Koga K, Zhang MM, Collingridge GL, Kaang BK, Zhuo M (2013) Long-term potentiation of synaptic transmission in the adult mouse insular cortex: multielectrode array recordings. J Neurophysiol 110(2):505–521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu MG, Song Q, Zhuo M (2018) Loss of synaptic tagging in the anterior cingulate cortex after tail amputation in adult mice. J Neurosci 38(37):8060–8070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Y, Chen QY, Lee JH, Li XH, Yu S, Zhuo M (2020) Cortical potentiation induced by calcitonin gene-related peptide (CGRP) in the insular cortex of adult mice. Mol Brain 13(1):36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loweth JA, Andrew F, Scheyer M, Milovanovic AL, LaCrosse E, Flores-Barrera CT, Werner X, Li KA, Ford T, Le MF, Olive KK, Szumlinski KY, Tseng Wolf TME (2014) Synaptic depression via mGluR1 positive allosteric modulation suppresses cue-induced cocaine craving. Nat Neurosci 17(1):73–80. https://doi.org/10.1038/nn.3590

  • Lu JS, Chen QY, Zhou S, Inokuchi K, Zhuo M (2018) Dual roles of anterior cingulate cortex neurons in pain and pleasure in adult mice. Mol Brain 11(1):72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maren S (1999) Long-term potentiation in the amygdala: a mechanism for emotional learning and memory. Trends Neurosci 22(12):561–567

    Article  CAS  PubMed  Google Scholar 

  • Miao HH, Li XH, Chen QY, Zhuo M (2019) Calcium-stimulated adenylyl cyclase subtype 1 is required for presynaptic long-term potentiation in the insular cortex of adult mice. Mol Pain 15:1744806919842961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao HH, Miao Z, Pan JG, Li XH, Zhuo M (2021) Brain-derived neurotrophic factor produced long-term synaptic enhancement in the anterior cingulate cortex of adult mice. Mol Brain 14(1):140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakoshi H, Wang H, Yasuda R (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472(7341):100–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Myers B, Greenwood-Van Meerveld B (2009) Role of anxiety in the pathophysiology of irritable bowel syndrome: importance of the amygdala. Front Neurosci 3:47

    Article  PubMed  PubMed Central  Google Scholar 

  • Navratilova E, Atcherley CW, Porreca F (2015) Brain circuits encoding reward from pain relief. Trends Neurosci 38(11):741–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen PV, Abel T, Kandel ER (1994) Requirement of a critical period of transcription for induction of a late phase of LTP. Science 265(5175):1104–1107

    Article  CAS  PubMed  Google Scholar 

  • Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355(1):27–37

    Article  CAS  PubMed  Google Scholar 

  • Nixon E, Liddle PF, Nixon NL, Liotti M (2013) On the interaction between sad mood and cognitive control: the effect of induced sadness on electrophysiological modulations underlying Stroop conflict processing. Int J Psychophysiol 87(3):313–326

    Article  PubMed  Google Scholar 

  • Osuch EA, Ketter TA, Kimbrell TA, George MS, Benson BE, Willis MW, Herscovitch P, Post RM (2000) Regional cerebral metabolism associated with anxiety symptoms in affective disorder patients. Biol Psychiatry 48(10):1020–1023

    Article  CAS  PubMed  Google Scholar 

  • Paoletti P, Bellone C, Zhou Q (2013) NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat Rev Neurosci 14(6):383–400

    Article  CAS  PubMed  Google Scholar 

  • Park P, Kang H, Sanderson TM, Bortolotto ZA, Georgiou J, Zhuo M, Kaang BK, Collingridge GL (2019) On the role of calcium-permeable AMPARs in long-term potentiation and synaptic tagging in the rodent hippocampus. Front Synaptic Neurosci 11:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patterson M, Yasuda R (2011) Signalling pathways underlying structural plasticity of dendritic spines. Br J Pharmacol 163(8):1626–1638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plant K, Pelkey KA, Bortolotto ZA, Morita D, Terashima A, McBain CJ, Collingridge GL, Isaac JT (2006) Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci 9(5):602–604

    Article  CAS  PubMed  Google Scholar 

  • Ploghaus A, Narain C, Beckmann CF, Clare S, Bantick S, Wise R, Matthews PM, Rawlins JN, Tracey I (2001) Exacerbation of pain by anxiety is associated with activity in a hippocampal network. J Neurosci 21(24):9896–9903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Redondo RL, Morris RG (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12(1):17–30

    Article  CAS  PubMed  Google Scholar 

  • Reymann KG, Frey JU (2007) The late maintenance of hippocampal LTP: requirements, phases, ‘synaptic tagging’, ‘late-associativity’ and implications. Neuropharmacology 52(1):24–40

    Article  CAS  PubMed  Google Scholar 

  • Robbins M, DeBerry J, Ness T (2007) Chronic psychological stress enhances nociceptive processing in the urinary bladder in high-anxiety rats. Physiol Behav 91(5):544–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rogan MT, Staubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390(6660):604–607

    Article  CAS  PubMed  Google Scholar 

  • Sanderson TM, Ralph LT, Amici M, Ng AN, Kaang BK, Zhuo M, Kim SJ, Georgiou J, Collingridge GL (2022) Selective recruitment of presynaptic and postsynaptic forms of mGluR-LTD. Front Synaptic Neurosci 14:857675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sewards TV, Sewards MA (2003) Representations of motivational drives in mesial cortex, medial thalamus, hypothalamus and midbrain. Brain Res Bull 61(1):25–49

    Article  PubMed  Google Scholar 

  • Shao XM, Sun J, Jiang YL, Liu BY, Shen Z, Fang F, Du JY, Wu YY, Wang JL, Fang JQ (2016) Inhibition of the cAMP/PKA/CREB pathway contributes to the analgesic effects of electroacupuncture in the anterior cingulate cortex in a rat pain memory model. Neural Plast 2016:5320641

    Article  PubMed  PubMed Central  Google Scholar 

  • Shibata H (1993) Efferent projections from the anterior thalamic nuclei to the cingulate cortex in the rat. J Comp Neurol 330(4):533–542

    Article  CAS  PubMed  Google Scholar 

  • Song Q, Zheng HW, Li XH, Huganir RL, Kuner T, Zhuo M, Chen T (2017) Selective phosphorylation of AMPA receptor contributes to the network of long-term potentiation in the anterior cingulate cortex. J Neurosci 37(35):8534–8548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Talbot JD, Marrett S, Evans AC, Meyer E, Bushnell MC, Duncan GH (1991) Multiple representations of pain in human cerebral cortex. Science 251(4999):1355–1358

    Article  CAS  PubMed  Google Scholar 

  • Tang J, Ko S, Ding HK, Qiu CS, Calejesan AA, Zhuo M (2005) Pavlovian fear memory induced by activation in the anterior cingulate cortex. Mol Pain 1:6

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomas, Rogerson DJ, Cai A, Frank Y, Sano J, Shobe MF, Lopez-Aranda AJ, Silva (2014) Synaptic tagging during memory allocation Nat Rev Neurosci 15(3):157–169. https://doi.org/10.1038/nrn3667

  • Thibault K, Lin WK, Rancillac A, Fan M, Snollaerts T, Sordoillet V, Hamon M, Smith GM, Lenkei Z, Pezet S (2014) BDNF-dependent plasticity induced by peripheral inflammation in the primary sensory and the cingulate cortex triggers cold allodynia and reveals a major role for endogenous BDNF as a tuner of the affective aspect of pain. J Neurosci 34(44):14739–14751

    Article  PubMed  PubMed Central  Google Scholar 

  • Tovote P, Fadok JP, Luthi A (2015) Neuronal circuits for fear and anxiety. Nat Rev Neurosci 16(6):317–331

    Article  CAS  PubMed  Google Scholar 

  • Toyoda H, Wu LJ, Zhao MG, Xu H, Jia Z, Zhuo M (2007a) Long-term depression requires postsynaptic AMPA GluR2 receptor in adult mouse cingulate cortex. J Cell Physiol 211(2):336–343

    Article  CAS  PubMed  Google Scholar 

  • Toyoda H, Wu LJ, Zhao MG, Xu H, Zhuo M (2007b) Time-dependent postsynaptic AMPA GluR1 receptor recruitment in the cingulate synaptic potentiation. Dev Neurobiol 67(4):498–509

    Article  CAS  PubMed  Google Scholar 

  • Toyoda H, Zhao MG, Mercaldo V, Chen T, Descalzi G, Kida S, Zhuo M (2010) Calcium/calmodulin-dependent kinase IV contributes to translation-dependent early synaptic potentiation in the anterior cingulate cortex of adult mice. Mol Brain 3:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Vardalaki D, Chung K, Harnett MT (2022) Filopodia are a structural substrate for silent synapses in adult neocortex. Nature 612(7939):323–327

    Article  CAS  PubMed  Google Scholar 

  • Wang HX, Gao WJ (2010) Development of calcium-permeable AMPA receptors and their correlation with NMDA receptors in fast-spiking interneurons of rat prefrontal cortex. J Physiol 588(Pt 15):2823–2838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang CC, Shyu BC (2004) Differential projections from the mediodorsal and centrolateral thalamic nuclei to the frontal cortex in rats. Brain Res 995(2):226–235

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Zhuo M (2012) Group I metabotropic glutamate receptor-mediated gene transcription and implications for synaptic plasticity and diseases. Front Pharm 3. https://doi.org/10.3389/fphar.2012.00189

  • Watters AJ, Korgaonkar MS, Carpenter JS, Harris AWF, Gross JJ, Williams LM (2018) Profiling risk for depressive disorder by circuit, behavior and self-report measures of emotion function. J Affect Disord 227:595–602

    Article  PubMed  Google Scholar 

  • Wayman GA, Lee YS, Tokumitsu H, Silva AJ, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59(6):914–931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei F, Zhuo M (2001) Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat. J Physiol 532(Pt 3):823–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei F, Li P, Zhuo M (1999) Loss of synaptic depression in mammalian anterior cingulate cortex after amputation. J Neurosci 19(21):9346–9354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, Xu HM, Chen ZF, Storm DR, Muglia LJ, Zhuo M (2002a) Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Neuron 36(4):713–726

    Article  CAS  PubMed  Google Scholar 

  • Wei F, Qiu CS, Liauw J, Robinson DA, Ho N, Chatila T, Zhuo M (2002b) Calcium calmodulin-dependent protein kinase IV is required for fear memory. Nat Neurosci 5(6):573–579

    Article  CAS  PubMed  Google Scholar 

  • Wen J, Xu Y, Yu Z, Zhou Y, Wang W, Yang J, Wang Y, Bai Q, Li Z (2022) The cAMP response element- binding protein/brain-derived neurotrophic factor pathway in anterior cingulate cortex regulates neuropathic pain and Anxiodepression like behaviors in rats. Front Mol Neurosci 15:831151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wise RG, Lujan BJ, Schweinhardt P, Peskett GD, Rogers R, Tracey I (2007) The anxiolytic effects of midazolam during anticipation to pain revealed using fMRI. Magn Reson Imaging 25(6):801–810

    Article  CAS  PubMed  Google Scholar 

  • Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FW, Zerbinatti CV, Bu G, Wei F, Xu TL, Muglia LJ, Chen ZF, Auberson YP, Kaang BK, Zhuo M (2005a) Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J Neurosci 25(48):11107–11116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu LJ, Zhao MG, Toyoda H, Ko SW, Zhuo M (2005b) Kainate receptor-mediated synaptic transmission in the adult anterior cingulate cortex. J Neurophysiol 94(3):1805–1813

    Article  CAS  PubMed  Google Scholar 

  • Wu LJ, Kim SS, Li X, Zhang F, Zhuo M (2009) Sexual attraction enhances glutamate transmission in mammalian anterior cingulate cortex. Mol Brain 2:9

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M (2008) Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. J Neurosci 28(29):7445–7453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamura H, Iwata K, Tsuboi Y, Toda K, Kitajima K, Shimizu N, Nomura H, Hibiya J, Fujita S, Sumino R (1996) Morphological and electrophysiological properties of ACCx nociceptive neurons in rats. Brain Res 735(1):83–92

    Article  CAS  PubMed  Google Scholar 

  • Yoshino A, Okamoto Y, Onoda K, Yoshimura S, Kunisato Y, Demoto Y, Okada G, Yamawaki S (2010) Sadness enhances the experience of pain via neural activation in the anterior cingulate cortex and amygdala: an fMRI study. NeuroImage 50(3):1194–1201

    Article  PubMed  Google Scholar 

  • Young JZ, Nguyen PV (2005) Homosynaptic and heterosynaptic inhibition of synaptic tagging and capture of long-term potentiation by previous synaptic activity. J Neurosci 25(31):7221–7231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao MG, Toyoda H, Ko SW, Ding HK, Wu LJ, Zhuo M (2005a) Deficits in trace fear memory and long-term potentiation in a mouse model for fragile X syndrome. J Neurosci 25(32):7385–7392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao MG, Toyoda H, Lee YS, Wu LJ, Ko SW, Zhang XH, Jia Y, Shum F, Xu H, Li BM, Kaang BK, Zhuo M (2005b) Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory. Neuron 47(6):859–872

    Article  CAS  PubMed  Google Scholar 

  • Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, Zhuo M (2006) Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. J Neurosci 26(35):8923–8930

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou Z, Ye P, Li XH, Zhang Y, Li M, Chen QY, Lu JS, Xue M, Li Y, Liu W, Lu L, Shi W, Xu PY, Zhuo M (2022) Correction to: synaptic potentiation of anterior cingulate cortex contributes to chronic pain of Parkinson’s disease. Mol Brain 15(1):58

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou SB, Xue M, Liu W, Chen YX, Chen QY, Lu JS, Wang J, Ye K, Li XH, Zhuo M (2023) Age-related attenuation of cortical synaptic tagging in the ACC is rescued by BDNF or a TrkB receptor agonist in both sex of mice. Mol Brain 16(1):4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhuo M (2008) Cortical excitation and chronic pain. Trends Neurosci 31(4):199–207

    Article  CAS  PubMed  Google Scholar 

  • Zhuo M (2012) Cortical depression and potentiation: basic mechanisms for phantom pain. Exp Neurobiol 21(4):129–135

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhuo M (2016) Neural mechanisms underlying anxiety-chronic pain interactions. Trends Neurosci 39(3):136–145

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zhuomin Institute of Brain Research, Qingdao, China

    Weiqi Liu, Qi-Yu Chen & Min Zhuo

  2. Center for Neuron and Disease, Frontier Institutes of Science and Technology, Xi’an Jiaotong University, Xi’an, China

    Weiqi Liu & Min Zhuo

  3. CAS Key Laboratory of Brain Connectome and Manipulation, Interdisciplinary Center for Brain Information, The Brain Cognition and Brain Disease Institute, Chinese Academy of Sciences Shenzhen Institute of Advanced Technology, Shenzhen, China

    Qi-Yu Chen

  4. Department of Physiology, Faculty of Medicine, University of Toronto, Toronto, ON, Canada

    Min Zhuo

Authors
  1. Weiqi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qi-Yu Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Min Zhuo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Min Zhuo .

Editor information

Editors and Affiliations

  1. Physiology and Health Longevity, National University of Singapore, Kent Ridge, Singapore

    Sreedharan Sajikumar

  2. Iowa Neuroscience Institute, University of Iowa, Iowa City, IA, USA

    Ted Abel

Rights and permissions

Reprints and permissions

Copyright information

© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Liu, W., Chen, QY., Zhuo, M. (2024). Synaptic Tagging in the ACC: Basic Mechanisms and Functional Implications. In: Sajikumar, S., Abel, T. (eds) Synaptic Tagging and Capture. Springer, Cham. https://doi.org/10.1007/978-3-031-54864-2_17

Download citation

Publish with us

Policies and ethics

Search

Navigation