Endocannabinoid signalling selectively targets perisomatic inhibitory inputs to pyramidal neurones in juvenile mouse neocortex

Journal of Physiology

Volumn 556, Issue 1, 2004, Pages 95-107

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

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; CANNABINOID DERIVATIVE; CANNABINOID RECEPTOR; MUSCARINIC RECEPTOR; CANNABINOID 1 RECEPTOR; ENDOCANNABINOID;

ANIMAL CELL; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; GABAERGIC SYSTEM; INFORMATION PROCESSING; INTERNEURON; MOUSE; NEOCORTEX; NERVE CELL MEMBRANE STEADY POTENTIAL; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REGULATORY MECHANISM; SENSORY CORTEX; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP; ADOLESCENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; NERVE CELL EXCITABILITY; NEUROMODULATION; SIGNAL TRANSDUCTION; SYNAPSE;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ELECTROPHYSIOLOGY; ENDOCANNABINOIDS; MICE; NEOCORTEX; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 1942517936     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2003.058198     Document Type: Article

References (52)

1. Beierlein M, Gibson JR & Connors BW (2000). A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat Neurosci 3, 904-910.
2. Beinfeld MC & Connolly K (2001). Activation of CB1 cannabinoid receptors in rat hippocampal slices inhibits potassium-evoked cholecystokinin release, a possible mechanism contributing to the spatial memory defects produced by cannabinoids. Neurosci Lett 301, 69-71.
3. Burdakov D & Ashcroft FM (2002). Cholecystokinin tunes firing of an electrically distinct subset of arcuate nucleus neurons by activating A-type potassium channels. J Neurosci 22, 6380-6387.
4. Chevaleyre V & Castillo PE (2003). Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38, 461-472.
5. Connors BW & Gutnick MJ (1990). Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13, 99-104.
6. Diana MA, Levenes C, Mackie K & Marty A (2002). Short-term retrograde inhibition of GABAergic synaptic currents in rat Purkinje cells is mediated by endogenous cannabinoids. J Neurosci 22, 200-208.
7. Di Marzo V, Melck D, Bisogno T & De Petrocellis L (1998). Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci 21, 521-528.
8. Egertova M & Elphick MR (2000). Localisation of cannabinoid receptors in the rat brain using antibodies to the intracellular C-terminal tail of CB. J Comp Neurol 422, 159-171.
9. Ferraro L, Tomasini MC, Cassano T, Bebe BW, Siniscalchi A, O'Connor WT, Magee P, Tanganelli S, Cuomo V & Antonelli T (2001). Cannabinoid receptor agonist WIN 55,212-2 inhibits rat cortical dialysate gamma-aminobutyric acid levels. J Neurosci Res 66, 298-302.
10. Freund TF, Katona I & Piomelli D (2003). Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83, 1017-1066.
11. Frisina R & Walton J (2001). Neuroanatomy of the central auditory system. In Handbook of Mouse Auditory Research: from Behavior to Molecular Biology, ed. Willott, J., pp. 243-277. CRC Press, Boca Raton.
12. Gerdeman GL, Ronesi J & Lovinger DM (2002). Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat Neurosci 5, 446-451.
13. Ghijsen WE, Leenders AG & Wiegant VM (2001). Regulation of cholecystokinin release from central nerve terminals. Peptides 22, 1213-1221.
14. Gupta A, Wang Y & Markram H (2000). Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science 287, 273-278.
15. Hampson RE, Zhuang SY, Weiner JL & Deadwyler SA (2003). Functional significance of cannabinoid-mediated, depolarization-induced suppression of inhibition (DSI) in the hippocampus. J Neurophysiol 90, 55-64.
16. Jentsch JD, Andrusiak E, Tran A, Bowers MB Jr & Roth RH (1997). Delta 9-tetrahydrocannabinol increases prefrontal cortical catecholaminergic utilization and impairs spatial working memory in the rat: blockade of dopaminergic effects with HA966. Neuropsychopharmacology 16, 426-432.
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. Kawaguchi Y (1997). Selective cholinergic modulation of cortical GABAergic cell subtypes. J Neurophysiol 78, 1743-1747.
19. Kawaguchi Y & Kubota Y (1996). Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 16, 2701-2715.
20. Kawaguchi Y & Kubota Y (1997). GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7, 476-486.
21. Kawaguchi Y & Kubota Y (1998). Neurochemical features and synaptic connections of large physiologically-identified GABAergic cells in the rat frontal cortex. Neuroscience 85, 677-701.
22. 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.
23. Kondo S & Kawaguchi Y (2001). Slow synchronized bursts of inhibitory postsynaptic currents (0.1-0.3 Hz) by cholinergic stimulation in the rat frontal cortex in vitro. Neuroscience 107, 551-560.
24. Kreitzer AC & Regehr WG (2001). Cerebellar depolarization-induced suppression of inhibition is mediated by endogenous cannabinoids. J Neurosci 21, RC174.
25. Kubota Y & Kawaguchi Y (1997). Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res 752, 175-183.
26. Larkum ME, Zhu JJ & Sakmann B (1999). A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338-341.
27. Llano I, Leresche N & Marty A (1991). Calcium entry increases the sensitivity of cerebellar Purkinie cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6, 565-574.
28. 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.
29. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, Cascio MG, Hermann H, Tang J, Hofmann C, Zieglgansberger W, Di Marzo V & Lutz B (2002). The endogenous cannabinoid system controls extinction of aversive memories. Nature 418, 530-534.
30. Martin LA & Alger BE (1999). Muscarinic facilitation of the occurrence of depolarization-induced suppression of inhibition in rat hippocampus. Neuroscience 92, 61-71.
31. A receptor-mediated IPSCs to depolarization-induced suppression of inhibition in rat hippocampus. J Physiol 532, 685-700.
32. McCormick DA, Connors BW, Lighthall JW & Prince DA (1985). Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54, 782-806.
33. Miles R, Toth K, Gulyas AI, Hajos N & Freund TF (1996). Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815-823.
34. Ohno-Shosaku T, Maejima T & Kano M (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29, 729-738.
35. Paxinos G & Franklin KBJ (2001). The Mouse Brain in Stereotaxic Coordinates. Academic Press, San Diego.
36. A responses in hippocampal pyramidal cells. J Neurosci 12, 4122-4132.
37. Pitler TA & Alger BE (1994). Depolarization-induced suppression of GABAergic inhibition in rat hippocampal pyramidal cells: G protein involvement in a presynaptic mechanism. Neuron 13, 1447-1455.
38. Robbe D, Kopf M, Remaury A, Bockaert J & Manzoni OJ (2002). Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc Natl Acad Sci U S A 99, 8384-8388.
39. Sebret A, Lena I, Crete D, Matsui T, Roques BP & Dauge V (1999). Rat hippocampal neurons are critically involved in physiological improvement of memory processes induced by cholecystokinin-B receptor stimulation. J Neurosci 19, 7230-7237.
40. Segev I & London M (1999). A theoretical view of passive and active dendrites. In Dendrites, ed. Stuart, G, Spruston, N & Hausser, M., pp. 205-230. Oxford University Press, New York.
41. Sjostrom PJ, Turrigiano GG & Nelson SB (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641-654.
42. Soltesz I, Smetters DK & Mody I (1995). Tonic inhibition originates from synapses close to the soma. Neuron 14, 1273-1283.
43. Somogyi P, Tamas G, Lujan R & Buhl EH (1998). Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 26, 113-135.
44. Steriade M (2000). Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101, 243-276.
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, 2334-2338.
47. Tsou K, Mackie K, Sanudo-Pena MC & Walker JM (1999). Cannabinoid CB1 receptors are localized primarily on cholecystokinin-containing GABAergic interneurons in the rat hippocampal formation. Neuroscience 93, 969-975.
48. Williams SR & Stuart GJ (2003). Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26, 147-154.
49. Wilson RI, Kunos G & Nicoll RA (2001). Presynaptic specificity of endocannabinoid signaling in the hippocampus. Neuron 31, 453-462.
50. Wilson RI & Nicoll RA (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.
51. Yoshida T, Hashimoto K, Zimmer A, Maejima T, Araishi K & Kano M (2002). The cannabinoid CB1 receptor mediates retrograde signals for depolarization-induced suppression of inhibition in cerebellar Purkinje cells. J Neurosci 22, 1690-1697.
52. Zilberter Y (2000). Dendritic release of glutamate suppresses synaptic inhibition of pyramidal neurons in rat neocortex. J Physiol 528, 489-496.