Conditional dendritic spike propagation following distal synaptic activation of hippocampal CA1 pyramidal neurons

Nature Neuroscience

Volumn 8, Issue 12, 2005, Pages 1667-1676

  Jarsky, Tim ^a   Roxin, Alex ^b,c   Kath, William L ^a,b   Spruston, Nelson ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Northwestern University   (United States)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER;

ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; COMPUTER MODEL; DENDRITE; HIPPOCAMPUS; MALE; NERVE CELL PLASTICITY; NERVE PROJECTION; NONHUMAN; PERFORANT NERVE TRACT; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; DENDRITES; HIPPOCAMPUS; LONG-TERM DEPRESSION (PHYSIOLOGY); LONG-TERM POTENTIATION; MALE; MEMORY; NEURAL INHIBITION; NEURAL NETWORKS (COMPUTER); NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; PERFORANT PATHWAY; PYRAMIDAL CELLS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION;

EID: 28044434108     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn1599     Document Type: Article

References (44)

1. Stuart, G., Spruston, N., Sakmann, B. & Häusser, M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20, 125-131 (1997).
2. Johnston, D., Magee, J.C., Colbert, C.M. & Christie, B.R. Active properties of neuronal dendrites. Annu. Rev. Neurosci. 19, 165-186 (1996).
3. Häusser, M., Spruston, N. & Stuart, G.J. Diversity and dynamics of dendritic signaling. Science 290, 739-744 (2000).
4. Amaral, D.G. Emerging principles of intrinsic hippocampal organization. Curr. Opin. Neurobiol. 3, 225-229 (1993).
5. Colbert, C.M. & Levy, W.B. Electrophysiological and pharmacological characterization of perforant path synapses in CA1: mediation by glutamate receptors. J. Neurophysiol. 68, 1-8 (1992).
6. Desmond, N.L., Scott, C.A., Jane, J.A., Jr. & Levy, W.B. Ultrastructural identification of entorhinal cortical synapses in CA1 stratum lacunosum-moleculare of the rat. Hippocampus 4, 594-600 (1994).
7. Levy, W.B., Colbert, C.M. & Desmond, N.L. Another network model bites the dust: entorhinal inputs are no more than weakly excitatory in the hippocampal CA1 region. Hippocampus 5, 137-140 (1995).
8. Soltesz, I. Brief history of cortico-hippocampal time with a special reference to the direct entorhinal input to CA1. Hippocampus 5, 120-124 (1995).
9. Yeckel, M.F. & Berger, T.W. Monosynaptic excitation of hippocampal CA1 pyramidal cells by afferents from the entorhinal cortex. Hippocampus 5, 108-114 (1995).
10. Golding, N.L. & Spruston, N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21, 1189-1200 (1998).
11. Kamondi, A., Acsady, L. & Buzsaki, G. Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J. Neurosci. 18, 3919-3928 (1998).
12. + channel densities in the soma and axon initial segment of subicular pyramidal neurons. J. Neurosci. 16, 6676-6686 (1996).
13. Spruston, N., Schiller, Y., Stuart, G. & Sakmann, B. Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297-300 (1995).
14. Golding, N.L., Kath, W.L. & Spruston, N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol. 86, 2998-3010 (2001).
15. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875 (1997).
16. + conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J. Comput. Neurosci. 7, 5-15 (1999).
17. Poirazi, P., Brannon, T. & Mel, B.W. Arithmetic of subthreshold synaptic summation in a model CA1 pyramidal cell. Neuron 37, 977-987 (2003).
18. Golding, N.L., Staff, N.P. & Spruston, N. Dendritic spikes as a mechanism for cooperative long-term potentiation. Nature 418, 326-331 (2002).
19. Goldstein, S.S. & Rall, W. Changes of action potential shape and velocity for changing core conductor geometry. Biophys. J. 14, 731-757 (1974).
20. Manor, Y., Koch, C. & Segev, I. Effect of geometrical irregularities on propagation delay in axonal trees. Biophys. J. 60, 1424-1437 (1991).
21. Stuart, G.J. & Hausser, M. Dendritic coincidence detection of EPSPs and action potentials. Nat. Neurosci. 4, 63-71 (2001).
22. Anderson, P., Storm, J. & Wheal, H.V. Thresholds of action potentials evoked by synapses on the dendrites of pyramidal cells in the rat hippocampus in vitro. J. Physiol. (Lond.) 383, 509-526 (1987).
23. Andersen, P. & Lomo, T. Mode of activation of hippocampal pyramidal cells by excitatory synapses on dendrites. Exp. Brain Res. 2, 247-260 (1966).
24. Buzsaki, G., Penttonen, M., Bragin, A., Nadasdy, Z. & Chrobak, J.J. Possible physiological role of the perforant path-CA1 projection. Hippocampus 5, 141-146 (1995).
25. Empson, R.M. & Heinemann, U. The perforant path projection to hippocampal area CA1 in the rat hippocampal-entorhinal cortex combined slice. J. Physiol. (Lond.) 484, 707-720 (1995).
26. Empson, R.M. & Heinemann, U. Perforant path connections to area CA1 are predominantly inhibitory in the rat hippocampal-entorhinal cortex combined slice preparation. Hippocampus 5, 104-107 (1995).
27. Remondes, M. & Schuman, E.M. Direct cortical input modulates plasticity and spiking in CA1 pyramidal neurons. Nature 416, 736-740 (2002).
28. Pare, D. & Llinas, R. Intracellular study of direct entorhinal inputs to field CA1 in the isolated guinea pig brain in vitro. Hippocampus 5, 115-119 (1995).
29. Doller, H.J. & Weight, F.F. Perforant pathway activation of hippocampal CA1 stratum pyramidale neurons: electrophysiological evidence for a direct pathway. Brain Res. 237, 1-13 (1982).
30. Yeckel, M.F. & Berger, T.W. Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. Proc. Natl. Acad. Sci. USA 87, 5832-5836 (1990).
31. Brun, V.H. et al. Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science 296, 2243-2246 (2002).
32. McNaughton, B.L., Barnes, CA., Meltzer, J. & Sutherland, R.J. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp. Brain Res. 76, 485-496 (1989).
33. Gasparini, S., Migliore, M. & Magee, J.C. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci. 24, 11046-11056 (2004).
34. Fellous, J.M., Rudolph, M., Destexhe, A. & Sejnowski, T.J. Synaptic background noise controls the input/output characteristics of single cells in an in vitro model of in vivo activity. Neuroscience 122, 811-829 (2003).
35. Frick, A., Magee, J. & Johnston, D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat. Neurosci. 7, 126-135 (2004).
36. Johnston, D., Hoffman, D.A., Colbert, C.M. & Magee, J.C. Regulation of back-propagating action potentials in hippocampal neurons. Curr. Opin. Neurobiol. 9, 288-292 (1999).
37. Spencer, W.A. & Kandel, E.R. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J. Neurophysiol. 24, 272-285 (1961).
38. Wong, R.K. & Stewart, M. Different firing patterns generated in dendrites and somata of CA1 pyramidal neurones in guinea-pig hippocampus. J. Physiol. (Lond.) 457, 675-687 (1992).
39. Cauller, L.J. & Connors, B.W. Functions of very distal dendrites: experimental and computational studies of layer I inputs to layer V pyramidal neurons in neocortex. in Single Neuron Computation (eds. McKenna, T., Davis, J. & Zornetzer, S.F.) 199-230 (Academic Press, San Diego, 1992).
40. Larkum, M.E., Senn, W. & Luscher, H.R. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14, 1059-1070 (2004).
41. Larkum, M.E., Zhu, J.J. & Sakmann, B. A new cellular mechanism for coupling inputs arriving at different cortical layers. Nature 398, 338-341 (1999).
42. Hines, M.L. & Carnevale, N.T. The NEURON simulation environment. Neural Comput. 9, 1179-1209 (1997).
43. Megias, M., Emri, Z., Freund, T.F. & Gulyas, A.I. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527-540 (2001).
44. Magee, J.C. & Cook, E.P. Somatic EPSPamplitude is independent of synapse location in hippocampal pyramidal neurons. Nat. Neurosci. 3, 895-903 (2000).