Forebrain NMDA receptors contribute to neuronal spike responses in adult mice

( views:95, downloads:0 )
Author:
WANG Guo-Du()
ZHUO Min()
Journal Title:
ACTA PHYSIOLOGICA SINICA
Issue:
Volume 58, Issue 06, 2006
DOI:
Key Word:
anterior cingulate cortex;NMDA receptor;adenylyl cyclase;action potential;cAMP;mice

Abstract: Glutamate is the major fast excitatory transmitter in the central nervous system.While normal synaptic transmission is mediated byα-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid(AMPA)and kainate receptors,N-methyl-D-aspartate(NMDA) receptors are thought to selectively contribute to plasticity.Genetically enhancing NMDA receptor functions enhances animal behavior in normal physiological learning and enhances their sensitivity in the case of tissue injury.One major mechanism for NMDA receptors is synaptic long-term potentiation(LTP).Here we present evidence that NMDA receptors not only contribute to normal synaptic responses induced by stimulation of local layer V or white matters,but also contribute to generation of action potentials induced by a depolarizing step applied to the soma.Calcium-calmodulin sensitive adenylyl cyclase 1 and cAMP signal pathways likely mediate these effects.Considering the importance of cingulate neurons in nociception and pain,our results provide a new mechanism for NMDA receptor contributing to neuronal synaptic transmission,spiking properties in forebrains,and possible forebrain-related behavioral nociceptive responses and pain.

  • [1]Zhuo M.Central inhibition and placebo analgesia.Mol Pain 2005:1:21.
  • [2]Zhuo M.Canadian Association of Neuroscience review:Cellular and synaptic insights into physiological and pathological pain.EJLB-CIHR Michael Smith Chair in Neurosciences and Mental Health lecture.Can J Neurol Sci 2005;32(1):27-36.
  • [3]Vogt BA.Pain and emotion interactions in subregions of the cingulate gyms.Nat Rev Neurosci 2005;6(7):533-544.
  • [4]Lee DE,Kim SJ,Zhuo M.Comparison of behavioral responses to noxious cold and heat in mice.Brain Res 1999;845(1):117-121.
  • [5]Johansen JP,Fields HL,Manning BH.The affective component of painin rodents:direct evidence for acontribution of the anterior cingulate cortex.Proc Natl Acad Sci USA 2001;98(14):8077-8082.
  • [6]Fbltz EL.White LE Jr.Pain"relief" by frontal cingulumotomy.J Neurosurg 1962;19:89-100.
  • [7]Hurt RW,Ballantine HT Jr.Stereotactic anterior cingulate lesions for persistent pain:a report on 68 cases.Clin Neurosurg 1974;21:334-351.
  • [8]Zhuo M.Glutamate receptors and persistentpain:targeting forebrain NR2B subunits.Drug Discov Today 2002;7(4):259-267.
  • [9]Sikes RW,Vogt BA.Nociceptive neurons in area 24 of rabbit cingulate cortex.J Neurophysiol 1992;68(5):1720-1732.
  • [10]Vogt BA SR,Vogt LJ.Anterior cingulate cortex and the medical pain system.In"Neurobiology of cingulate cogex and limbic thalamus:a comprehensive handbook".Vogt BA GM.ed.Boston:Birkhauser,1993.313-344.
  • [11]Traub RJ,Silva E,Gebhart GF,Solodkin A.Noxious colorectal distention induced-c-Fos protein in limbic brain structures in the rat.Neurosci Lett 1996;215(3):165-168.
  • [12]Hutchison WD,Davis KD,Lozano AM,Tasker RR,Dostrovsky JO.Pain-related neurons in the human cingulate codex.Nat Neurosci 1999;2(5):403-405.
  • [13]Wei F.Zhuo M.Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat.J Physiol 2001;532(Pt 3):823-833.
  • [14]Wei F,Li P,Zhuo M.Loss of synaptic depression in malnnlalian anterior cingulate cortex after amputation.J Neurosci 1999;19 (21):9346-9354.
  • [15]Wei F,Qiu CS,Kim SJ,Muglia L,Maas JW,Pineda VV,Xu HM,Chen ZF,Storm DR,Muglia LJ,Zhuo M.Genetic elimina tion of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases.Neuron 2002;36(4):713-726.
  • [16]Kuo CC,Yen CT.Comparison of anterior cingulate and primary somatosensory neuronal responses to noxious laser-heat stimuli in conscious,behaving rats.J Neurophysiol 2005;94(3):1825-1836.
  • [17]Rainville P,Duncan GH,Price DD,Carrier B,Bushnell MC.Pain affect encoded inhuman anterior cingulate but not somatosensory cortex.Science 1997;277(5328):968-971.
  • [18]Rainville P.Brain mechanisms of pain affect and pain modulation.Curt Opin Neurobiol 2002;12(2):195-204.
  • [19]Talbot JD,Marrett S,Evans AC,Meyer E,Bushnell MC,Duncan GH.Multiple representations of pain in human cerebral cortex,Science 1991:251(4999):1355-1358.
  • [20]Vogt BA,Derbyshire S,Jones AK.Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging.Eur J Neurosci 1996;8(7):1461-1473.
  • [21]Casey KL.Forebrain mechanisms of nociception and pain:analysis through imaging.Proc Natl Acad Sci USA 1999;96(14):7668-7674.
  • [22]Calejesan AA,Kim SJ,Zhuo M.Descending facifitatory modulation of a behavioral nociceptive response by stimulation in the adult ratanterior cingulate cortex.Eur J Pain2000;4(1):83-96.
  • [23]Tang J,Ko S,Ding HK,Qiu CS,Calejesan AA,ZhuoM.Pavlovian fear memory induced by activation in the anterior cingulate cortex.Mol Pain 2005;1(1):6.
  • [24]Bliss TV.Collingridge GL.A synaptic model of memory:longterm potentiation in the hippocampus.Nature 1993;361(6407):31-39.
  • [25]Collingridge GL,Bliss TV.Memories of NMDA receptors and LTP.Trends Neurosci 1995;18(2):54-56.
  • [26]Monyer H,Bumashev N,Laurie DJ,Sakmann B,Seeburg PH.Developmental and regional expression in the ratbrain and functional properties of four NMDA receptors.Neuron 1994;12(3):529-540.
  • [27]Wei F,Wang GD,Kerchner GA,Kim SJ,Xu HM,Chen ZF,Zhuo M.Genetic enhancement of inflammatory pain by forebrain NR2B overexpression.Nat Neurosci 2001;4(2):164-169.
  • [28]Boyce S,Wyau A,Webb JK,O'Donnell R,Mason G,Rigby M,Sirinathsinghji D,Hill RG,Rupniak NM.Selective NMDA NR2B antagonists induce antinOciception without motor dysfunction:correlation with restricted localisation of NR2B subunit in dorsal horn.Neuropharmacology 1999;38(5):611-623.
  • [29]Tao YX,Rumbaugh G,Wang GD,Petralia RS,Zhao C,Kauer FW,Tao F,Zhuo M,Wenthold RJ,Raja SN,Huganir RL,Bredt DS.Johns RA.Impaired NMDA receptor-mediated postsynaptic function and blunted NMDA receptor-dependent persistent pain in mice lacking postsynaptic density-93 protein.J Neurosci 2003:23(17):6703-6712.
  • [30]Bliss TV.Young receptors make smart mice.Nature 1999;401 (6748):25-27.
  • [31]Tang YP,Shimizu E,Dube GR,Rampon C,Kerchner GA,Zhuo M,Liu G,Tsien JZ.Genetic enhancement of learning and memory in mice.Nature 1999;401(6748):63-69.
  • [32]Liauw J.Wu LJ.Zhuo M.Calcium-stimulated adenylyl cyclases required for long-term potentiation in the anterior cingulate cortex.J Neurophysiol 2005;94(1):878-882.
  • [33]Liauw J,Wang GD,Zhuo M.NMDA receptors contribute to synaptic transmission in anterior cingulate cortex of adultmice.Acta Physiol Sin(生理学报)2003;55(4):373-380.
  • [34]Wang GD,Zhuo M.Synergistic enhancement of glutamate-mediated responses by serotonin and for skolin in adultmouse spinal dorsal horn neurons.J Neurophysiol 2002;87(2):732-739.
  • [35]Wang CC,Shyu BC.Differential projections from the mediodorsal and centrolateral thalamic nuclei to the frontal cortexin rats.Brain Res 2004;995(2):226-235.
  • [36]Xia Z,Storm DR.Calmodulin-regulated adenylyl cyclases and neuromodulation.Curr Opin Neurobiol 1997;7(3):391-396.
  • [37]Villacres EC,Wong ST,Chavkin C,Storm DR.Type I adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation.J Neurosci 1998;18(9):3186-3194.
  • [38]Wei F,Qiu CS,Liauw J,Robinson DA,Ho N,Chatila T,Zhuo M.Calcium calmodulin-dependent protein kinase Ⅳ is required for fear memory.Nat Neurosci 2002;5(6):573-579.
  • [39]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.Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation.J Neurosci 2005;25(48):11107-11116.
  • [40]Sah P,Hestrin S,Nicoll RA.Tonic activation of NMDA receptorsby ambient glutamate enhances excitability of neurons.Science 1989;246(4931):815-818.
  • [41]Gil Z.Amitai Y.Adult thalamocortical transmission involves both NMDA and non-NMDA receptors.J Neurophysiol 1996;76(4):2547-2554.
  • [42]Schiller J.Major G,Koester HJ,Schiller Y.NMDA spikes in basal dendrites of cortical pyramidal neurons.Nature 2000;404(6775):285-289.
  • [43]Kemp JA KJ.Gill R.NMDA receptor antagonists and their potential as neuroprotective agents.Handbook of Experimental Pharmacology 141:Ionotropic Glutamate Receptors in the CNS.Berlin:Springer-Verlag,1999.
  • [44]Wong ST,Athos J,Figueroa XA,Pineda VV,Schaefer ML,Chavkin CC,Muglia LJ,Storm DR.Calcium-stimulated adenylyl cyclase activity is critical for hippocampus-dependent long-term memory and late phase LTP.Neuron 1999;23(4):787-798.
  • [45]Zhao MG,Toyoda H,Lee YS,Wu LJ,Ko SW,Zhang XH Jia Y,Shum F,Xu H,Li BM,Kaang BK,Zhuo M.Roles of NMDA NR2B subtype receptor in prefrontal long-term potentiation and contextual fear memory.Neuron 2005;47(6):859-872.
  • [46]Xia Z,Choi EJ,Wang F,Blazynski C,Storm DR.Type I calmodulin-sensitive adenylyl cyclase is neural specific.J Neurochem 1993;60(1):305-311.
  • [47]Xia ZG,Refsdal CD,Merchant KM,Dorsa DM,Storm DR.Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain:expression in areas associated with 1earning and memory.Neuron 1991;6(3):431-443.
  • [48]Defer N,Best-Belpomme M,Hanoune J.Tissue specificity and physiological relevance of various isoforms of adenylyl cyclase.Am J Physiol Renal Physiol 2000:279(3):F400-F416.
  • [49]Devinsky O,Morrell MJ,Vogt BA.Contributions of anterior cingnlate cortex to behaviour.Brain 1995;118(Pt 1):279-306.
  • [50]Johansen JP.Fields HL.Glutamatergic activation of anterior cingulate cortex produces an aversive teaching signal.NatNeurosci 2004;7(4):398-403.
  • [51]Craig AD,Reiman EM,Evans A,Bushnell MC.Functional imaging of an illusion of pain.Nature 1996;384(6606):258-260.
  • [52]Davis KD.Taylor SJ.Crawley AP.Wood ML,Mikulis DJ.Functional MRI of pain-and attention-related activations in the human cingulate cortex.J Neurophysiol 1997;77(6):3370-3380.
  • [53]Derbyshire SW,Vogt BA,Jones AK.Pain and Stroop interference tasks activate separate processing modules in anterior cingulate cortex.Exp Brain Res 1998;118(1):52-60.
  • [54]Koyama T,Tanaka YZ,Mikami A.Nociceptive neurons in the macaque anterior cingulate activate during anticipation of pain.Neuroreport 1998;9(11):2663-2667.
  • [55]Li P,Kerchner GA,Sala C,Wei F,Huettner JE,Sheng M,Zhuo M.AMPA receptor-PDZ interactions in facilitation of spinal sensory synapses.Nat Neurosci 1999;2(11):972-977.
  • [56]Yamitsky D,Barron SA,Bental E.Disappearance of phantom pain after focal brain infarction.Pain 1988;32(3):285-287.
  • [57]Pastoriza LN,Morrow TJ,Casey KL.Medial frontal codex lesions selectively attenuate the hot plate response:possible nocifensive apraxia in the rat.Pain 1996;64(1):11-17.
WanfangData CO.,Ltd All Rights Reserved
About WanfangData | Contact US
Healthcare Department, Fuxing Road NO.15, Haidian District Beijing, 100038 P.R.China
Tel:+86-010-58882616 Fax:+86-010-58882615 Email:yiyao@wanfangdata.com.cn