Endocannabinoid release modulates electrical coupling between CCK cells connected via chemical and electrical synapses in CA1

Frontiers in Neural Circuits

Volumn 5, Issue NOV, 2011, Pages

  Iball, Jonathan ^a   Ali, Afia B ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

CA1; CB1; CCK; DSI; Electrically coupled; Endocannabinoids; Interneurons

Indexed keywords

BIOCYTIN; CANNABINOID 1 RECEPTOR; CHOLECYSTOKININ; ENDOCANNABINOID;

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENTATE GYRUS; ELECTRICAL COUPLING; HIPPOCAMPAL CA1 REGION; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LATENT PERIOD; MALE; NERVE CELL; NERVE FIBER; NERVE PROJECTION; NEUROMODULATION; NONHUMAN; RAT; STIMULUS RESPONSE; STRATUM RADIATUM; SYNAPSE;

EID: 84869498682     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncir.2011.00017     Document Type: Article

References (42)

1. Ali, A. B. (2007). Presynaptic inhibition of GABAA receptor-mediated unitary IPSPs by cannabinoid receptors at synapses between CCK-positive interneurons in rat hippocampus. J. Neurophysiol. 98, 861-869.
2. Ali, A. B. (2011). CB1 modulation of temporally distinct synaptic facilitation among local circuit interneu-rons mediated by N-type calcium channels in CA1. J. Neurophysiol. 105, 1051-1062.
3. Ali, A. B., Bannister, A. P., and Thomson, A. M. (1999). IPSPs elicited in CA1 pyramidal cells by putative basket cells in slices of adult rat hippocampus. Eur. J. Neurosci. 11, 1741-1753.
4. Ali, A. B., and Todorova, M. (2010). Asynchronous release of GABA via tonic cannabinoid receptor activation at identified interneuron synapses in rat CA1. Eur. J. Neurosci. 31, 1196-1207.
5. Best, A. R., and Regehr, W. G. (2009), Inhibitory regulation of electrically coupled neurons in the inferior olive is mediated by asynchronous release of GABA. Neuron 62, 555-565.
6. Blatow, M., Rozov, A., Katona, I., Hormuzdi, S. G., Meyer, A. H., Whit-tington, M. A., Caputi, A., and Monyer, H. (2003). A novel network of multipolar bursting interneu-rons generates theta frequency oscillations in neocortex. Neuron 38, 805-817.
7. Bodor, A. L., Katona, I., Nyiri, G., Mackie, K., Ledent, C., Hajos, N., and Freund, T. F. (2005). Endocannabinoid signaling in rat somatosensory cortex: laminar differences and involvement of specific interneuron types. J. Neurosci. 25, 6845-6856.
8. Caputi, A., Rozov, A., Blatow, M., and Monyer, H. (2009). Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb. Cortex 19, 1345-1359.
9. Chu, Z., Galarreta, M., and Hestrin, S. (2003). Synaptic interactions of late-spiking neocortical neurons in layer 1. J. Neurosci. 23, 96-102.
10. Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., and Somogyi, P. (1995). Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75-78.
11. Daw, M. I., Pelkey, K. A., Chittajallu, R., and McBain, C. J. (2010). Presynaptic kainate receptor acti vation preserves asynchronous GABA release despite the reduc tion in synchronous release from hippocampal cholecystokinin interneurons. J. Neurosci. 30, 11202-11209.
12. Freund, T. F., and Buzsaki, G. (1996). Interneurons of the hippocampus. Hippocampus 6, 347-470.
13. Galarreta, M., Erdelyi, F., Szabo, G., and Hestrin, S. (2004). Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J. Neurosci. 24, 9770-9778.
14. Galarreta, M., Erdelyi, F., Szabo, G., and Hestrin, S. (2008). Cannabi-noid sensitivity and synaptic properties of 2 GABAergic networks in the neocortex. Cereb. Cortex 18, 2296-2305.
15. Galarreta, M., and Hestrin, S. (1999). A network of fast-spiking cells in the neocortex connected by electrical synapses. Nature 402, 72-75.
16. Gibson, J. R., Beierlein, M., and Connors, B. W. (1999). Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402, 75-79.
17. Glickfeld, L. L., and Scanziani, M. (2006). Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat. Neurosci. 9, 807-815.
18. Hajós, M., Hoffmann, W. E., and Kocsis, B. (2008). Activation of cannabinoid-1 receptors disrupts sensory gating and neuronal oscillation: relevance to schizophrenia. Biol. Psychiatry 63, 1075-1083.
19. Hajós, N., Katona, I., Naiem, S. S., Mackie, K., Ledent, C., Mody, I., and Freund, T. F. (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci. 12, 3239-3249.
20. Hefft, S., and Jonas, P. (2005). Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 8, 1319-1328.
21. Hjorth, J., Blackwell, K. T., and Kotaleski, J. H. (2009). Gap junctions between striatal fast-spiking interneurons regulate spiking activity and synchronizations a function of cortical activity. J. Neurosci. 29, 5276-5286.
22. Hormuzdi, S. G., Pais, I., LeBeau, F. E., Towers, S. K., Rozov, A., Buhl, E. H., Whittington, M. A., and Monyer, H. (2001). Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31, 487-495.
23. Karson, M. A., Tang, A. H., Mil-ner, T. A., and Alger, B. E. (2009). Synaptic cross talk between perisomatic targeting interneuron classes expressing cholecystokinin and parvalbumin in hippocampus. J. Neurosci. 29, 4140-4154.
24. Katona, I., Sperlagh, B., Sik, A., Kafalvi, A., Vizi, E. S., Mackie, K., and Freund, T. F. (1999). Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneu-rons. J. Neurosci. 19, 4544-4558.
25. Kim, H., and Jones, K. E. (2011). Asymmetric electrotonic coupling between the soma and dendrites alters the bistable firing behaviour of reduced models. J. Comput. Neu-rosci. 30, 659-674.
26. Koos, T., and Tepper, J. M. (1999). Inhibitory control of neostriatal projection neurons by GABAer-gic interneurons. Nat. Neurosci. 2, 467-472.
27. Kosaka, T., and Hama, K. (1985). Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions): a combined Golgi-electron microscopy study. J. Comp. Neurol. 231, 150-161.
28. Kubota, Y., and Kawaguchi, Y. (1997). Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons. Brain Res. 752, 175-183.
29. Llano, I., Leresche, N., and Marty, A. (1991). Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6, 565-574.
30. Losonczy, A., Biro, A. A., and Nusser, Z. (2004). Persistently active cannabi-noid receptors mute a subpopulation of hippocampal interneurons. Proc. Natl. Acad. Sci. U.S.A. 101, 1362-1367.
31. Mancilla, J. G., Lewis, T. J., Pinto, D. J., Rinzel, J., and Connors, B. W. (2007). Synchronization of electrically coupled pairs of inhibitory interneu-rons in neocortex. J. Neurosci. 27, 2058-2073.
32. Marsicano, G., and Lutz, B. (1999). Expression of the cannabinoid receptor CB1 in distinct neuronal subpopulations in the adult mouse forebrain. Eur. J. Neurosci. 11, 4213-4225.
33. Ohno-Shosaku, T., Maejima, T., and Kano, M. (2001). Endogenous cannabinoids mediate retrograde signals from depolarized postsynap-tic neurons to presynaptic terminals. Neuron 29, 729-738.
34. Pappas, G.D., and Bennett, M.V.(1966). Specialized junctions involved in electrical transmission between neurons. Ann. N. Y. Acad. Sci. 137, 495-508.
35. Pawelzik, H., Hughes, D. I., and Thomson, A. M. (2002). Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J. Comp. Neurol. 443, 346-367.
36. Robbe, D., Montgomery, S. M., Thome, A., Rueda-Orozco, P. E., McNaughton, B. L., and Buzsaki, G. (2006). Cannabinoids reveal importance of spike timing coordination in hippocampal function. Nat. Neurosci. 9, 1526-1533.
37. Simon, A., Olah, S., Molnar, G., Szabadics, J., and Tamas, G. (2005). Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J. Neurosci. 25, 6278-6285.
38. Sloper, J. J. (1972). Gap junctions between dendrites in the primate neocortex. Brain Res. 44, 641-646.
39. Somogyi, P., and Klausberger, T. (2005). Defined types of cortical interneurone structure space and spike timing in the hippocampus. J. Physiol. (Lond.) 562, 9-26.
40. Tamas, G., Buhl, E. H., Lorincz, A., and Somogyi, P. (2000). Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons. Nat. Neurosci. 3, 366-371.
41. Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D., and Monyer, H. (2000). Connexin expression in electrically coupled postnatal rat brain neurons. Proc. Natl. Acad. Sci. U.S.A. 97, 10260-10265.
42. Wilson, R. I., and Nicoll, R. A. (2001). Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410, 588-592.