Differential effects of endocannabinoids on glutamatergic and GABAergic inputs to layer 5 pyramidal neurons

Cerebral Cortex

Volumn 17, Issue 1, 2007, Pages 163-174

  Fortin, Dale A ^a   Levine, Eric S ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Cannabinoid; DSE; DSI; Neocortex; Synapse

Indexed keywords

4 AMINOBUTYRIC ACID; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID; GLUTAMIC ACID;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DEPOLARIZATION; MOUSE; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM SIGNALING; DATA INTERPRETATION, STATISTICAL; ELECTROPHYSIOLOGY; ENDOCANNABINOIDS; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMATES; MICE; MORPHOLINES; NAPHTHALENES; NEURONAL PLASTICITY; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTOR, CANNABINOID, CB1; SYNAPTIC TRANSMISSION;

EID: 33845745763     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhj133     Document Type: Article

References (55)

1. Alger BE. 2002. Retrograde signaling in the regulation of synaptic transmission: focus on endocannabinoids. Prog Neurobiol 68:247-286.
2. Auclair N, Otani S, Soubrie P, Crepel F. 2000. Cannabinoids modulate synaptic strength and plasticity at glutamatergic synapses of rat prefrontal cortex pyramidal neurons. J Neurophysiol 83:3287-3293.
3. Bacci A, Huguenard JR, Prince DA. 2004. Long-lasting self-inhibition of neocortical interneurons mediated by endocannabinoids. Nature 431:312-316.
4. Berger MA, Defagot MC, Villar MJ, Antonelli MC. 2001. D4 dopamine and metabotropic glutamate receptors in cerebral cortex and striatum in rat brain. Neurochem Res 26:345-352.
5. Birtoli B, Ulrich D. 2004. Firing mode-dependent synaptic plasticity in rat neocortical pyramidal neurons. J Neurosci 24:4935-4940.
6. Bodor AL, Katona I, Nyiri G, Mackie K, Ledent C, Hajos N, Freund TF. 2005. Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J Neurosci 25:6845-6856.
7. Connors BW, Gutnick MJ, Prince DA. 1982. Electrophysiological properties of neocortical neurons in vitro. J Neurophysiol 48:1302-1320.
8. Defagot MC, Villar MJ, Antonelli MC. 2002. Differential localization of metabotropic glutamate receptors during postnatal development. Dev Neurosci 24:272-282.
9. Dodt HU, Schierloh A, Eder M, Zieglgansberger W. 2003. Circuitry of rat barrel cortex investigated by infrared-guided laser stimulation. Neuroreport 14:623-627.
10. Egertova M, Cravatt BF, Elphick MR. 2003. Comparative analysis of fatty acid amide hydrolase and cb(1) cannabinoid receptor expression in the mouse brain: evidence of a widespread role for fatty acid amide hydrolase in regulation of endocannabinoid signaling. Neuroscience 119:481-496.
11. Feldmeyer D, Egger V, Lubke J, Sakmann B. 1999. Reliable synaptic connections between pairs of excitatory layer 4 neurones within a single 'barrel' of developing rat somatosensory cortex. J Physiol 521(Pt 1):169-190.
12. Ferraro L, Tomasini MC, Gessa GL, Bebe BW, Tanganelli S, Antonelli T. 2001. The cannabinoid receptor agonist WIN 55,212-2 regulates glutamate transmission in rat cerebral cortex: an in vivo and in vitro study. Cereb Cortex 11:728-733.
13. Fortin DA, Trettel J, Levine ES. 2004. Brief trains of action potentials enhance pyramidal neuron excitability via endocannabinoid-mediated suppression of inhibition. J Neurophysiol 92:2105-2112.
14. Gulyas AI, Cravatt BF, Bracey MH, Dinh TP, Piomelli D, Boscia F, Freund TF. 2004. Segregation of two endocannabinoid-hydrolyzing enzymes into pre- and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. Eur J Neurosci 20:441-458.
15. Hajos N, Ledent C, Freund TF. 2001. Novel cannabinoid-sensitive receptor mediates inhibition of glutamatergic synaptic transmission in the hippocampus. Neuroscience 106:1-4.
16. Helmchen F, Svoboda K, Denk W, Tank DW. 1999. In vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons. Nat Neurosci 2:989-996.
17. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF. 1999. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci 19:4544-4558.
18. Kim J, Isokawa M, Ledent C, Alger BE. 2002. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci 22:10182-10191.
19. Kreitzer AC, Regehr WG. 2001a. Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21:RC174.
20. Kreitzer AC, Regehr WG. 2001b. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29:717-727.
21. Larkum ME, Zhu JJ, Sakmann B. 1999. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398:338-341.
22. Lisman JE. 1997. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20:38-43.
23. Llinas RR. 1988. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654-1664.
24. Maejima T, Hashimoto K, Yoshida T, Aiba A, Kano M. 2001. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31:463-475.
25. Maejima T, Ohno-Shosaku T, Kano M. 2001. Endogenous cannabinoid as a retrograde messenger from depolarized postsynaptic neurons to presynaptic terminals. Neurosci Res 40:205-210.
26. Marsicano G, Goodenough S, Monory K, Hermann H, Eder M, Cannich A, Azad SC, Cascio MG, Gutierrez SO, van der Stelt M, Lopez-Rodriguez ML, Casanova E, Schutz G, Zieglgansberger W, Di Marzo V, Behl C, Lutz B. 2003. CB1 cannabinoid receptors and on-demand defense against excitotoxicity. Science 302:84-88.
27. Marsicano G, Lutz B. 1999. Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur J Neurosci 11:4213-4225.
28. Matsuda LA, Bonner TI, Lolait SJ. 1993. Localization of cannabinoid receptor mRNA in rat brain. J Comp Neurol 327:535-550.
29. Melis M, Pistis M, Perra S, Muntoni AL, Pillolla G, Gessa GL. 2004. Endocannabinoids mediate presynaptic inhibition of glutamatergic transmission in rat ventral tegmental area dopamine neurons through activation of CB1 receptors. J Neurosci 24:53-62.
30. Mountcastle VB. 1997. The columnar organization of the neocortex. Brain 120(Pt 4):701-722.
31. Ohno-Shosaku T, Shosaku J, Tsubokawa H, Kano M. 2002. Cooperative endocannabinoid production by neuronal depolarization and group I metabotropic glutamate receptor activation. Eur J Neurosci 15:953-961.
32. Ohno-Shosaku T, Tsubokawa H, Mizushima I, Yoneda N, Zimmer A, Kano M. 2002. Presynaptic cannabinoid sensitivity is a major determinant of depolarization-induced retrograde suppression at hippocampal synapses. J Neurosci 22:3864-3872.
33. Patel S, Gerrits R, Muthian S, Greene AS, Hillard CJ. 2002. The CB1 receptor antagonist SR141716 enhances stimulus-induced activation of the primary somatosensory cortex of the rat. Neurosci Lett 335:95-98.
34. Paxinos G, Franklin KBJ. 2001. The mouse brain in stereotaxic coordinates. San Diego, CA: Academic Press.
35. Pontzer NJ, Hosko MJ, Wilkison DM. 1986. Alteration of electrical correlates of sensory processing by tetrahydrocannabinol. Exp Neurol 91:127-135.
36. Sherman SM, Guillery RW. 1996. Functional organization of thalamocortical relays. J Neurophysiol 76:1367-1395.
37. Silva LR, Amitai Y, Connors BW. 1991. Intrinsic oscillations of neocortex generated by layer 5 pyramidal neurons. Science 251:432-435.
38. Sjostrom PJ, Turrigiano GG, Nelson SB. 2003. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39:641-654.
39. Sjostrom PJ, Turrigiano GG, Nelson SB. 2004. Endocannabinoid-dependent neocortical layer-5 LTD in the absence of postsynaptic spiking. J Neurophysiol 92:3338-3343.
40. Stella N, Piomelli D. 2001. Receptor-dependent formation of endogenous cannabinoids in cortical neurons. Eur J Pharmacol 425:189-196.
41. Stratford KJ, Tarczy-Hornoch K, Martin KA, Bannister NJ, Jack JJ. 1996. Excitatory synaptic inputs to spiny stellate cells in cat visual cortex. Nature 382:258-261.
42. Swadlow HA, Gusev AG. 2001. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat Neurosci 4:402-408.
43. Thomson AM, West DC, Wang Y, Bannister AP. 2002. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2-5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labelling in vitro. Cereb Cortex 12:936-953.
44. Trettel J, Fortin DA, Levine ES. 2004. Endocannabinoid signalling selectively targets perisomatic inhibitory inputs to pyramidal neurones in juvenile mouse neocortex. J Physiol 556:95-107.
45. Trettel J, Levine ES. 2002. Cannabinoids depress inhibitory synaptic inputs received by layer 2/3 pyramidal neurons of the neocortex. J Neurophysiol 88:534-539.
46. Trettel J, Levine ES. 2003. Endocannabinoids mediate rapid retrograde signaling at interneuron → pyramidal neuron synapses of the neocortex. J Neurophysiol 89(4):2334-2338.
47. Tsou K, Brown S, Sanudo-Pena MC, Mackie K, Walker JM. 1998. Immunohistochemical distribution of cannabinoid CB1 receptors in the rat central nervous system. Neuroscience 83:393-411.
48. van der Stelt M, Veldhuis WB, Maccarrone M, Bar PR, Nicolay K, Veldink GA, Di Marzo V, Vliegenthart JF. 2002. Acute neuronal injury, excitotoxicity, and the endocannabinoid system. Mol Neurobiol 26:317-346.
49. Varma N, Carlson GC, Ledent C, Alger BE. 2001. Metabotropic glutamate receptors drive the endocannabinoid system in hippocampus. J Neurosci 21:RC188.
50. Wallace MJ, Blair RE, Falenski KW, Martin BR, DeLorenzo RJ. 2003. The endogenous cannabinoid system regulates seizure frequency and duration in a model of temporal lobe epilepsy. J Pharmacol Exp Ther 307:129-137.
51. Wilkison DM, Pontzer N, Hosko MJ. 1982. Slowing of cortical somatosensory evoked activity by delta 9-tetrahydrocannabinol and dimethylheptylpyran in alpha-chloralose-anesthetized cats. Neuropharmacology 21:705-709.
52. Wilson RI, Kunos G, Nicoll RA. 2001. Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31:453-462.
53. Wilson RI, Nicoll RA. 2001. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410:588-592.
54. Zhuang S, Hampson RE, Deadwyler SA. 2005. Behaviorally relevant endocannabinoid action in hippocampus: dependence on temporal summation of multiple inputs. Behav Pharmacol 16:463-471.
55. Zilberter Y, Harkany T, Holmgren CD. 2005. Dendritic release of retrograde messengers controls synaptic transmission in local neocortical networks. Neuroscientist 11:334-344.