Skip to main content
Log in

Selective axonal and glial distribution of monoacylglycerol lipase immunoreactivity in the superficial spinal dorsal horn of rodents

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

The importance of 2-AG-mediated endogenous cannabinoid signaling in spinal pain control has recently been well substantiated. Although the degradation of 2-AG seems to be essential in cannabinoid-mediated spinal nociceptive information processing, no experimental data are available about the cellular distribution of monoacylglycerol lipase (MGL), the main degrading enzyme of 2-AG in the spinal dorsal horn. Thus, here we investigated the cellular distribution of MGL in laminae I–II of the spinal gray matter with immunocytochemical methods and revealed an abundant immunoreactivity for MGL in the rodent superficial spinal dorsal horn. We addressed the co-localization of MGL with markers of peptidergic and non-peptidergic primary afferents, axon terminals of putative glutamatergic and GABAergic spinal neurons, as well as astrocytic and microglial profiles, and we found that nearly 17 % of the peptidergic (immunoreactive for CGRP), a bit more than 10 % of the axon terminals of putative glutamatergic spinal neurons (immunoreactive for VGLUT2), and approximately 20 % of the astrocytic (immunoreactive for GFAP) profiles were immunolabeled for MGL. On the other hand, however, axon terminals of non-peptidergic (binding isolectin-B4) nociceptive primary afferents and putative inhibitory spinal neurons (immunoreactive for VGAT) as well as microglial (immunoreactive for CD11b) profiles showed negligible immunostaining for MGL. The results suggest that only nociceptive inputs arriving through a population of CGRP immunoreactive fibers are modulated by the spinal DGLα–MGL pathway. We also postulate that the DGLα–MGL signaling pathway may modulate spinal excitatory but not inhibitory neural circuits.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Alger BE (2012) Endocannabinoids at the synapse a decade after the dies mirabilis (29 March 2001): what we still do not know. J Physiol 590:2203–2212

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Alvarez FJ, Villalra RM, Zerda R, Schneider SP (2004) Vesicular glutamate transporter in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472:257–280

    Article  CAS  PubMed  Google Scholar 

  • Araque A, Carmignoto G, Haydon PG (2001) Dynamic signaling between neurons and glia. Annu Rev Physiol 63:795–813

    Article  CAS  PubMed  Google Scholar 

  • Beltramo M, Piomelli D (2000) Carrier-mediated transport and enzymatic hydrolysis of the endogenous cannabinoid 2-arachidonylglycerol. Neuroreport 11:1231–1235

    Article  CAS  PubMed  Google Scholar 

  • Blankman JL, Simon GM, Cravatt BF (2007) A comprehensive profile of brain enzymes that hydrolyze the endocannabinoid 2-arachidonoylglycerol. Chem Biol 14:1347–1356

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Brumovsky P, Watanabe M, Hökfelt T (2007) Expression of the vesicular glutamate transporter-1 and -2 in adult mouse dorsal root ganglia and spinal cord and their regulation by nerve injury. Neuroscience 147:469–490

    Article  CAS  PubMed  Google Scholar 

  • Cabral GA, Marciano-Cabral F (2005) Cannabinoid receptors in microglia of the central nervous system: immune functional relevance. J Leukoc Biol 78:1192–1197

    Article  CAS  PubMed  Google Scholar 

  • Cao H, Zhang YQ (2008) Spinal glia activation contributes to pathological pain states. Neurosci Behav Rev 32:972–983

    Article  Google Scholar 

  • Chanda PK, Gao Y, Mark L, Joan Btesh J, Strassle BW, Lu P, Piesla MJ, Zhang MJ, Bingham B, Uveges A, Kowal D, Garbe D, Kouranova EV, Ring RH, Bates B, Pangalos MN, Kennedy JD, Whiteside GT, Samad TA (2010) Monoacylglycerol lipase activity is a critical modulator of the tone and integrity of the endocannabinoid system. Mol Pharmacol 78:996–1003

    Article  CAS  PubMed  Google Scholar 

  • Chang L, Luo L, Palmer JA, Sutton S, Wilson SJ, Barbier AJ, Breitenbucher JG, Chaplan SR, Webb M (2006) Inhibition of fatty acid amide hydrolase produces analgesia by multiple mechanisms. Br J Pharmacol 148:102113

    Google Scholar 

  • Chaudhry FA, Reimer RJ, Bellocchio EE, Danbolt NC, Osen KK, Edwards RH, Storm-Mathisen J (1998) The vesicular GABA transporter, VGAT, localizes to synaptic vesicles in sets of glycinergic as well as GABAergic neurons. J Neurosci 18:9733–9750

    CAS  PubMed  Google Scholar 

  • Chevaleyre V, Takahashi KA, Castillo PE (2006) Endocannabinoid-mediated synaptic plasticity in the CNS. Ann Rev Neurosci 29:37–76

    Article  CAS  PubMed  Google Scholar 

  • Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci USA 98:9371–9376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Di S, Popescu IR, Tasker JG (2013) Glial control of endocannabinoid heterosynaptic modulation in hypothalamic magnocellular neuroendocrine cells. J Neurosci 33:18331–18342

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dinh TP, Carpenter D, Leslie FM, Freund TF, Katona I, Sensi SL, Kathuria S, Piomelli D (2002) Brain monoglyceride lipase participating in endocannabinoid inactivation. Proc Natl Acad Sci USA 99:10819–10824

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Eriksson NP, Persson JK, Svensson M, Arvidsson J, Molander C, Aldskogius H (1993) A quantitative analysis of the microglial cell reaction in central primary sensory projection territories following peripheral nerve injury in the adult rat. Exp Brain Res 96:9–27

    Article  Google Scholar 

  • Fowler C, Tiger G (2005) Cyclooxygenation of the arachidonoyl side chain of 1-arachidonoylglycerol and related compounds block their ability to prevent anandamide and 2-oleoylglycerol metabolism by rat brain in vitro. Biochem Pharmacol 69:1241–1245

    Article  CAS  PubMed  Google Scholar 

  • Freund TF, Katona I, Piomelli D (2003) Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83:1017–1066

    Article  CAS  PubMed  Google Scholar 

  • Garrison CJ, Dougherty PM, Kajander KC, Carlton SM (1991) Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res 565:1–7

    Article  CAS  PubMed  Google Scholar 

  • Gordon GR, Iremonger KJ, Kantevari S, Ellies-Davies GC, MacVicar BA, Bains JS (2009) Astrocyte-mediated distributed plasticity at hypothalamic glutamate synapses. Neuron 64:391–403

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Graeber MB (2010) Changing face of microglia. Science 330:783–788

    Article  CAS  PubMed  Google Scholar 

  • Gulyás AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund F (2004) Segregation of two endocannabinoid-hydrolyzing enzyme into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdale. Eur J Neurosci 20:441–458

    Article  PubMed  Google Scholar 

  • Guo A, Vulchanova L, Wang J, Li X, Elde R (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11:946–958

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Yoshida T, Sakimura K, Mishina M, Watanabe M, Kano M (2008) Influence of parallel fiber-Purkinje cell synapse formation on postnatal development of climbing fiber-Purkinje cell synapses in the cerebellum. Neuroscience 162:601–611

    Article  PubMed  Google Scholar 

  • Hashimotodani Y, Ohno-Shosaku T, Kano M (2007) Ca2+-associated receptor driven endocannabinoid release: mechanisms that associate presynaptic and postsynaptic activities. Curr Opin Neurobiol 17:360–365

    Article  CAS  PubMed  Google Scholar 

  • Haydon PG, Carmingnoto G (2006) Astrocyte control of synaptic transmission and neurovascular coupling. Physiol Rev 86:1009–1031

    Article  CAS  PubMed  Google Scholar 

  • Hegyi Z, Kis G, Holló K, Leden C, Antal M (2009) Neuronal and glial localization of the cannabinoid-1 receptor in the superficial spinal dorsal horn of the rodent spinal cord. Eur J Neurosci 30:251–262

    Article  PubMed  Google Scholar 

  • Hegyi Z, Holló K, Kis G, Mackie K, Antal M (2012) Differential distribution of diacylglycerol lipase-alpha and N-acylphosphatidylethanolamine-specific phospholipase D immunoreactivity in the superficial spinal dorsal horn of rats. Glia 60:1316–1329

    Article  PubMed Central  PubMed  Google Scholar 

  • Kano M, Ohno-Shosaku T, Hashimotodani Y, Uchigashima M, Watanabe M (2009) Endocannabinoid-mediated control of synaptic transmission. Physiol Rev 89:309–380

    Article  CAS  PubMed  Google Scholar 

  • Kinsey SG, Long JZ, O’Neal ST, Abdullah RA, Poklis JL, Boger DL, Cravatt BF, Lichtman AH (2009) Blockade of endocannabinoid-degrading enzymes attenuates neuropathic pain. J Pharmacol Exp Ther 330:902–910

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kogan NM, Mechoulam R (2006) The chemistry of endocannabinoids. J Endocrinol Invest 29(Suppl. 3):3–14

    CAS  PubMed  Google Scholar 

  • Kozak KR, Crews BC, Morrow JD, Wang LH, Ma YH, Weinander R, Jakobsson PJ, Marnett LJ (2002) Metabolism of the endocannabinoids, 2-arachidonylglycerol and anandamide, into prostaglandin, thromboxane, and prostacyclin glycerol esters and ethanolamides. J Biol Chem 277:44877–44885

    Article  CAS  PubMed  Google Scholar 

  • Kozak KR, Prusakiewicz JJ, Marnett LJ (2004) Oxidative metabolism of endocannabinoids by COX-2. Curr Pharm Des 10:659–667

    Article  CAS  PubMed  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    Article  CAS  PubMed  Google Scholar 

  • Lambert DM, Fowler CJ (2005) The endocannabinoid system: drug targets, lead compounds, and potential therapeutic applications. J Med Chem 48:5059–5087

    Article  CAS  PubMed  Google Scholar 

  • Li JL, Fujimaya F, Kaneko T, Mizuno N (2003) Expression of vesicular glutamate transporters, VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat. J Comp Neurol 457:236–249

    Article  CAS  PubMed  Google Scholar 

  • Long JZ, Li W, Booker L, Burston JJ, Kinsey SG, Schlosburg JE, Pavón FJ, Serrano AM, Selley DE, Parsons LH, Lichtman AH, Cravatt BF (2009) Selective blockade of 2-arachidonoylglycerol hydrolysis produces cannabinoid behavioral effects. Nat Chem Biol 5:37–44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Makara JK, Mor M, Fegley D, Szabó SI, Kathuria S, Astarita G, Duranti A, Tontini A, Tarzia G, Rivara S, Freund TF, Piomelli D (2005) Selective inhibition of 2-AG hydrolysis enhances endocannabinoid signaling in hippocampus. Nat Neurosci 8:1139–1141

    Article  CAS  PubMed  Google Scholar 

  • McClung JR, Castro AJ (1978) Rexed's laminar scheme as it applies to the rat cervical spinal cord. Exp Neurol 58:145–148

    Article  CAS  PubMed  Google Scholar 

  • McNeil DL, Chung K, Hulsebosch CE, Bolander RP, Coggeshall RE (1988) Numbers of synapses in laminae I-IV of the rat dorsal horn. J Comp Neurol 278:453–460

    Article  Google Scholar 

  • Mechoulam R, Ben-Shabat S, Hanus L, Ligunsky M, Kaminski NE, Schatz AR, Gopher A, Almog S, Martin BR, Compton DR (1995) Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem Pharmacol 50:83–90

    Article  CAS  PubMed  Google Scholar 

  • Molander C, Xu Q, Grant G (1984) The cytoerchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J Comp Neurol 230:133–141

    Article  CAS  PubMed  Google Scholar 

  • Molander C, Hongpaisan J, Evensson M, Aldskogius H (1997) Glial cell reactions in the spinal cord after sensory nerve stimulation are associated with axonal injury. Brain Res 747:122–129

    Article  CAS  PubMed  Google Scholar 

  • Murataeva N, Straiker A, Mackie K (2014) Parsing the players: 2-arachidonoylglycerol synthesis and degradation in the CNS. Br J Pharmacol 171:1379–1391

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nasu F (1999) Analysis of calcitonin gene-related peptide (CGRP)-containing nerve fibres in the rat spinal cord using light and electron microscopy. J Electron Microsc 48:267–275

    Article  CAS  Google Scholar 

  • Navarrate M, Araque A (2008) Endocannabinoids mediate neuron-astrocyte communication. Neuron 57:883–893

    Article  Google Scholar 

  • Nedergaard M, Ransom B, Goldman SA (2003) New roles for astrocytes: redefining the functional architecture of the brain. Trends Neurosci 26:523–530

    Article  CAS  PubMed  Google Scholar 

  • Nyilas R, Gregg LC, Mackie K, Watanabe M, Zimmer A, Hohmann AG, Katona I (2009) Molecular architecture of endocannabinoid signaling at nociceptive synapses mediating analgesia. Eur J Neurosci 29:1964–1978

    Article  PubMed Central  PubMed  Google Scholar 

  • Oliveira ALR, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hökfelt T, Cullheim S, Meister B (2003) Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50:117–129

    Article  CAS  PubMed  Google Scholar 

  • Pan B, Wang W, Long JZ, Sun D, Hillard CJ, Cravatt BF, Liu QS (2009) Blockade of 2-arachidonoylglycerol hydrolysis by selective monoacylglycerol lipase inhibitor 4-nitrophenyl 4-(dibenzo[d][1,3]dioxil-5yl(hydroxyl)methyl) piperidine-1carboxylate (JZL184) enhances retrograde endocannabinoid signaling. J Pharmacol Exp Ther 331:591–597

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pan B, Wang W, Zhong P, Blankman JL, Cravatt BF, Liu QS (2011) Alterations of endocannabinoid signaling, synaptic plasticity, learning, and memory in monoacylglycerol lipase knock-out mice. J Neurosci 31:13420–13430

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Patricelli MP, Cravatt BF (2001) Proteins regulating the biosynthesis and inactivation of neuromodulatory fatty acid amides. Vitam Horm 62:95–131

    Article  CAS  PubMed  Google Scholar 

  • Piet R, Vargová L, Syková E, Poulain DA, Oliet SH (2004) Physiological contribution of the astrocytic environment of neurons to intersynaptic crosstalk. Proc Natl Acad Sci USA 101:2151–2155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Polgar E, Todd AJ (2008) Tactile allodynia can occur in the spared nerve injury model in the rat without selective loss of GABA or GABA(A) receptors from synapses in laminae I–II of the ipsilateral spinal dorsal horn. Neurosciemce 156:193–202

    Article  CAS  Google Scholar 

  • Ribeiro da Silva A, De Korninck Y (2009) Morphological and neurochemical organization of the spinal dorsal horn. In: Basbaum AI, Bushnell MC (eds) Science of pain. Elsevier, Oxford, pp 279–310

    Google Scholar 

  • Rodriquez JJ, Mackie K, Pickel VM (2001) Ultrastructural localization of the CB1 cannabinoid receptor in mu-opioid receptor patches of the rat caudate putamen nucleus. J Neurosci 21:823–833

    Google Scholar 

  • Salio C, Doly S, Fischer J, Franzoni MF, Conrath M (2002) Neuronal and astrocytic localization of the cannabinoid receptor-1 in the dorsal horn of the rat spinal cord. Neurosci Lett 329:13–16

    Article  CAS  PubMed  Google Scholar 

  • Schlosburg JE, Blankman JL, Long JZ, Nomura DK, Pan B, Kinsey SG, Nguyen PT, Ramesh D, Booker L, Burston JJ, Thomas EA, Selley DE, Sim-Selley LJ, Liu QS, Lichtman AH, Cravatt BF (2010) Chronic monoacylglycerol lipase blockade causes functional antagonism of the endocannabinoid system. Nat Neurosci 13:1113–1119

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scholz J, Woolf CJ (2007) The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 11:1361–1368

    Article  Google Scholar 

  • Starowicz K, Makuch W, Korostynski M, Malek N, Slezak M, Zychowska M, Petrosino S, De Petrocellis L, Cristino L, Przewlocka B, Di Marzo V (2013) Full inhibition of spinal FAAH leads to TRPV1-mediated analgesic effects in neuropathic rats and possible lipoxygenase-mediated remodeling of anandamide metabolism. PLoS One 8:e60040

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stella N (2009) Endocannabinoid signaling in microglial cells. Neuropharmacol 56(Suppl 1):244–253

    Article  CAS  Google Scholar 

  • Straiker A, Mackie K (2009) Cannabinoid signaling in inhibitory autaptic hippocampal neurons. Neuroscience 163:190–201

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Straiker A, Hu SS, Long JZ, Arnold A, Wager-Miller J, Cravatt BF, Mackie K (2009) Monoacylglycerol lipase limits the duration of endocannabinoid-mediated depolarization-induced suppression of excitation in autaptic hippocampal neurons. Mol Pharmacol 76:1220–1227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sugiura T, Kondo S, Sukagawa A, Nakane S, Shinoda A, Itoh K, Yamashita A, Waku K (1995) 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem Biophys Res Commun 215:89–97

    Article  CAS  PubMed  Google Scholar 

  • Suter MR, Wen YR, Decosterd I, Ji RR (2007) Do glial cells control pain? Neuron Glia Biol 3:255–268

    Article  PubMed Central  PubMed  Google Scholar 

  • Szabo B, Urbanski MJ, Bisogno T, Di Marzo V, Mendiguren A, Baer WU, Freiman I (2006) Depolarization-induced retrograde synaptic inhibition in the mouse cerebellar cortex is mediated by 2-arachidonoylglycerol. J Physiol 577:263–280

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tanimura A, Uchigasima M, Yamazaki M, Uesaka N, Mikuni T, Abe M, Hashimoto K, Watanabe M, Sakimura K, Kano M (2012) Synapse type-independent degradation of the endocannabinoid 2-arachidonoylglycerol after retrograde synaptic suppression. PNAS 109:12195–12200

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tasker JG, Oliet SH, Bains JS, Brown CH, Stern JE (2012) Glial regulation of neuronal function: from synapse to systems physiology. J Neuroendocrinol 24:566–576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Todd AJ, Hughes DI, Polgár E, Nagy GG, Mackie M, Ottersen OP, Maxwell DJ (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17:13–27

    Article  CAS  PubMed  Google Scholar 

  • Traub RJ, Solodkin A, Ruda MA (1989) Calcitonin gene-related peptide immunoreactivity in the cat lumbosacral spinal cord and the effects of multiple dorsal rhizotomies. J Comp Neurol 287:225–237

    Article  CAS  PubMed  Google Scholar 

  • Uchigasima M, Yamazaki M, Yamasaki M, Tanimura A, Sakimura K, Kano M, Watanabe M (2011) Molecular and morphological configuration for 2-arachidonoylglycerol-mediated retrograde signaling at mossy cell-granule cell synapses in the dentate gyrus. J Neurosci 31:7700–7714

    Article  Google Scholar 

  • van der Stelt M, Noordermeer MA, Kiss T, Van Zadelhoff G, Merghart B, Veldink GA, Vliegenthart JF (2000) Formation of a new class of oxylipins from N-acyl(ethanol)amines by the lipoxygenase pathway. Eur J Biochem 267:2000–2007

    Article  Google Scholar 

  • Vandevoorde S, Lambert DM (2007) The multiple pathways of endocannabinoid metabolism: a zoom out. Chem Biodivers 4:1858–1881

    Article  CAS  PubMed  Google Scholar 

  • Volterra A, Bezzi P (2002) The tripartite synapse: Glia. In: Volterra A, Magistretti PJ, Haydon PG (eds) Synaptic transmission. Oxford UP, New York, pp 164–168

    Google Scholar 

  • Walter L, Stella L (2003) Endothelin-1 increases 2-arachidonyl glycerol (2-AG) production in astrocytes. Glia 44:85–90

    Article  PubMed  Google Scholar 

  • Walter L, Dinh T, Stella N (2004) ATP induces a rapid and pronounced increase in 2-arachidonylglycerol production by astrocytes, a response limited by monoacylglycerol lipase. J Neurosci 24:8068–8074

    Article  CAS  PubMed  Google Scholar 

  • Willis WD, Coggeshall RE (2004) Sensory mechanisms of the spinal cord, vol 1., Primary afferent neurons and the spinal dorsal hornKluwer Academic/Plenum Publishers, New York

    Book  Google Scholar 

  • Witting A, Walter L, Wacker J, Moller T, Stella N (2004) P2X7 receptors control 2-arachidonoylglycerol production by microglial cells. Proc Natl Acad Sci USA 101:3214–3219

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Woodhams SG, Wong A, Barrett DA, Bennett AJ, Chapman V, Alexander SP (2012) Spinal administration of the monoacylglycerol lipase inhibitor JZL184 produces robust inhibitory effects on nociceptive processing and the development of central sensitization in the rat. Br J Pharmacol 167:1609–1619

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang F, Vadakkan KI, Kim SS, Wu LJ, Shang Y, Zhuo M (2008) Selective activation of microglia in spinal cord but not higher cortical regions following nerve injury in adult mouse. Mol Pain 4:1–16

    Article  Google Scholar 

  • Zohng P, Pan B, Gao XP, Blankman JL, Cravatt BF, Liu QS (2011) Genetic deletion of monoacylglycerol lipase alters endocannabinoid-mediated retrograde synaptic depression in the cerebellum. J Physiol 589:4847–4855

    Article  Google Scholar 

Download references

Acknowledgments

The authors are thankful to Ken Mackie (Department of Psychological and Brain Sciences, Indiana University, Bloomington, Indiana, USA) for kindly providing spinal cord samples from MGL knock out mice for the experiments. This work was supported by the Hungarian Academy of Sciences (MTA-TKI 242) and the Hungarian Brain Research Program (Grant No. KTIA_13_NAP-A-I/8).

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Miklós Antal.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dócs, K., Hegyi, Z., Holló, K. et al. Selective axonal and glial distribution of monoacylglycerol lipase immunoreactivity in the superficial spinal dorsal horn of rodents. Brain Struct Funct 220, 2625–2637 (2015). https://doi.org/10.1007/s00429-014-0813-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-014-0813-x

Keywords

Navigation