Dynamics of action potential backpropagation in basal dendrites of prefrontal cortical pyramidal neurons

European Journal of Neuroscience

Volumn 27, Issue 4, 2008, Pages 923-936

  Zhou, Wen Liang ^a   Yan, Ping ^a   Wuskell, Joseph P ^a   Loew, Leslie M ^a   Antic, Srdjan D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Distal dendritic segments; Imaging; Prefrontal cortex; Rat; Voltage sensitive dyes

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACK PROPAGATION; BASAL GANGLION; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITE; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; IMAGING; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; WAVEFORM;

ACTION POTENTIALS; ANIMALS; CALCIUM SIGNALING; DENDRITES; ELECTROPHYSIOLOGY; IMAGE PROCESSING, COMPUTER-ASSISTED; ORGAN CULTURE TECHNIQUES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 40549090281     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06075.x     Document Type: Article

References (61)

1. Antic, S.D. (2003) Action potentials in basal and oblique dendrites of rat neocortical pyramidal neurons. J. Physiol. (Lond.), 550, 35 50.
2. Antic, S., Major, G. Zecevic, D. (1999) Fast optical recordings of membrane potential changes from dendrites of pyramidal neurons. J. Neurophysiol., 82, 1615 1621.
3. Araya, R., Eisenthal, K.B. Yuste, R. (2006) Dendritic spines linearize the summation of excitatory potentials. Proc. Natl Acad. Sci. USA, 103, 18799 18804.
4. Benavides-Piccione, R., Hamzei-Sichani, F., Ballesteros-Yanez, I., DeFelipe, J. Yuste, R. (2006) Dendritic size of pyramidal neurons differs among mouse cortical regions. Cereb. Cortex, 16, 990 1001.
5. Burkhalter, A. (1989) Intrinsic connections of rat primary visual cortex: laminar organization of axonal projections. J. Comp. Neurol., 279, 171 186.
6. Chafee, M.V. Goldman-Rakic, P.S. (1998) Matching patterns of activity in primate prefrontal area 8a and parietal area 7ip neurons during a spatial working memory task. J. Neurophysiol., 79, 2919 2940.
7. Chang, J.Y., Janak, P.H. Woodward, D.J. (2000) Neuronal and behavioral correlations in the medial prefrontal cortex and nucleus accumbens during cocaine self-administration by rats. Neuroscience, 99, 433 443.
8. Dan, Y. Poo, M.M. (2004) Spike timing-dependent plasticity of neural circuits. Neuron, 44, 23 30.
9. Elston, G.N. (2003) Cortex, cognition and the cell: New insights into the pyramidal neuron and prefrontal function. Cereb. Cortex, 13, 1124 1138.
10. Elston, G.N., Benavides-Piccione, R. DeFelipe, J. (2001) The pyramidal cell in cognition: a comparative study in human and monkey. J Neurosci., 21, RC163.
11. Enoki, R., Kiuchi, T., Koizumi, A., Sasaki, G., Kudo, Y. Miyakawa, H. (2004) NMDA receptor-mediated depolarizing after-potentials in the basal dendrites of CA1 pyramidal neurons. Neurosci. Res., 48, 325 333.
12. Feldmeyer, D., Lubke, J., Silver, R.A. Sakmann, B. (2002) Synaptic connections between layer 4 spiny neurone-layer 2/3 pyramidal cell pairs in juvenile rat barrel cortex: physiology and anatomy of interlaminar signalling within a cortical column. J. Physiol. (Lond.), 538, 803 822.
13. Gasparini, S., Losonczy, A., Chen, X., Johnston, D. Magee, J.C. (2007) Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons. J. Physiol. (Lond.), 580, 289 302.
14. Gasparini, S., Migliore, M. Magee, J.C. (2004) On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J. Neurosci., 24, 11046 11056.
15. Golding, N.L., Kath, W.L. Spruston, N. (2001) Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol., 86, 2998 3010.
16. Goldman-Rakic, P.S. (1995) Cellular basis of working memory. Neuron, 14, 477 485.
17. Gordon, U., Polsky, A. Schiller, J. (2006) Plasticity compartments in basal dendrites of neocortical pyramidal neurons. J. Neurosci., 26, 12717 12726.
18. Gulledge, A.T. Jaffe, D.B. (1998) Dopamine decreases the excitability of layer V pyramidal cells in the rat prefrontal cortex. J. Neurosci., 18, 9139 9151.
19. Holthoff, K., Kovalchuk, Y. Konnerth, A. (2006) Dendritic spikes and activity-dependent synaptic plasticity. Cell Tissue Res., 326, 369 377.
20. Homayoun, H. Moghaddam, B. (2006) Bursting of prefrontal cortex neurons in awake rats is regulated by metabotropic glutamate 5 (mGlu5) receptors: rate-dependent influence and interaction with NMDA receptors. Cereb. Cortex, 16, 93 105.
21. Jaffe, D.B., Johnston, D., Lasser-Ross, N., Lisman, J.E., Miyakawa, H. Ross, W.N. (1992) The spread of Na+ spikes determines the pattern of dendritic Ca2+ entry into hippocampal neurons. Nature, 357, 244 246.
22. Kampa, B.M., Letzkus, J.J. Stuart, G.J. (2006) Requirement of dendritic calcium spikes for induction of spike-timing-dependent synaptic plasticity. J. Physiol. (Lond.), 574, 283 290.
23. Kampa, B.M. Stuart, G.J. (2006) Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts. J. Neurosci., 26, 7424 7432.
24. Koester, H.J. Sakmann, B. (1998) Calcium dynamics in single spines during coincident pre- and postsynaptic activity depend on relative timing of back-propagating action potentials and subthreshold excitatory postsynaptic potentials. Proc. Natl Acad. Sci. USA, 95, 9596 9601.
25. Kritzer, M.F. Goldman-Rakic, P.S. (1995) Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in the rhesus monkey. J. Comp. Neurol., 359, 131 143.
26. Larkman, A.U. (1991) Dendritic morphology of pyramidal neurones of the visual cortex of the rat. III. Spine distributions. J. Comp. Neurol., 306, 332 343.
27. Larkum, M.E., Kaiser, K.M. Sakmann, B. (1999) Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc. Natl Acad. Sci. USA, 96, 14600 14604.
28. Larkum, M.E., Zhu, J.J. Sakmann, B. (2001) Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J. Physiol. (Lond.), 533, 447 466.
29. Letzkus, J.J., Kampa, B.M. Stuart, G.J. (2006) Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. J. Neurosci., 26, 10420 10429.
30. Levitt, J.B., Lewis, D.A., Yoshioka, T. Lund, J.S. (1993) Topography of pyramidal neuron intrinsic connections in macaque monkey prefrontal cortex (areas 9 and 46). J. Comp. Neurol., 338, 360 376.
31. Linden, D.J. (1999) The return of the spike: postsynaptic action potentials and the induction of LTP and LTD. Neuron, 22, 661 666.
32. Lisman, J., Malenka, R.C., Nicoll, R.A. Malinow, R. (1997) Learning mechanisms: the case for CaM-KII. Science, 276, 2001 2002.
33. London, M., Schreibman, A., Hausser, M., Larkum, M.E. Segev, I. (2002) The information efficacy of a synapse. Nat. Neurosci., 5, 332 340.
34. Lubke, J., Roth, A., Feldmeyer, D. Sakmann, B. (2003) Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb. Cortex, 13, 1051 1063.
35. Magee, J.C. Johnston, D. (1997) A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science, 275, 209 213.
36. Markram, H. (1997) A network of tufted layer 5 pyramidal neurons. Cereb. Cortex, 7, 523 533.
37. Markram, H., Lubke, J., Frotscher, M. Sakmann, B. (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science, 275, 213 215.
38. Migliore, M. Shepherd, G.M. (2002) Emerging rules for the distributions of active dendritic conductances. Nat. Rev. Neurosci., 3, 362 370.
39. Milojkovic, B.A., Radojicic, M.S. Antic, S.D. (2005a) A strict correlation between dendritic and somatic plateau depolarizations in the rat prefrontal cortex pyramidal neurons. J. Neurosci., 25, 3940 3951.
40. Milojkovic, B.A., Wuskell, J.P., Loew, L.M. Antic, S.D. (2005b) Initiation of sodium spikelets in basal dendrites of neocortical pyramidal neurons. J. Membr. Biol., 208, 155 169.
41. Milojkovic, B.A., Zhou, W.L. Antic, S.D. (2007) Voltage and calcium transients in basal dendrites of the rat prefrontal cortex. J. Physiol. (Lond.), 585, 447 468.
42. Morishima, M. Kawaguchi, Y. (2006) Recurrent connection patterns of corticostriatal pyramidal cells in frontal cortex. J. Neurosci., 26, 4394 4405.
43. Nevian, T., Larkum, M.E., Polsky, A. Schiller, J. (2007) Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat. Neurosci., 10, 206 214.
44. 2+ signaling in spike-timing-dependent plasticity. J. Neurosci., 26, 11001 11013.
45. Oakley, J.C., Schwindt, P.C. Crill, W.E. (2001) Dendritic calcium spikes in layer 5 pyramidal neurons amplify and limit transmission of ligand-gated dendritic current to soma. J. Neurophysiol., 86, 514 527.
46. Polsky, A., Mel, B.W. Schiller, J. (2004) Computational subunits in thin dendrites of pyramidal cells. Nat. Neurosci., 7, 621 627.
47. Ramus, S.J. Eichenbaum, H. (2000) Neural correlates of olfactory recognition memory in the rat orbitofrontal cortex. J. Neurosci., 20, 8199 8208.
48. Rapp, M., Yarom, Y. Segev, I. (1996) Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. Proc. Natl Acad. Sci. USA, 93, 11985 11990.
49. Rhodes, P.A. (1999) Functional implications of active currents in the dendrites of pyramidal neuros. In Ulinski, P.S. Jones, E.G. (eds), Cerebral Cortex. Kluwer Academic/ Plenum Publishers, New York, pp. 139 200.
50. Ross, W.N., Salzberg, B.M., Cohen, L.B., Grinvald, A., Davila, H.V., Waggoner, A.S. Wang, C.H. (1977) Changes in absorption, fluorescence, dichroism, and Birefringence in stained giant axons: optical measurement of membrane potential. J. Membr. Biol., 33, 141 183.
51. Schiller, J., Major, G., Koester, H.J. Schiller, Y. (2000) NMDA spikes in basal dendrites of cortical pyramidal neurons. Nature, 404, 285 289.
52. Sjostrom, P.J. Hausser, M. (2006) A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron, 51, 227 238.
53. Spruston, N., Schiller, Y., Stuart, G. Sakmann, B. (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science, 268, 297 300.
54. Staiger, J.F., Kotter, R., Zilles, K. Luhmann, H.J. (2000) Laminar characteristics of functional connectivity in rat barrel cortex revealed by stimulation with caged-glutamate. Neurosci. Res., 37, 49 58.
55. Stuart, G., Schiller, J. Sakmann, B. (1997) Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. (Lond.), 505, 617 632.
56. Thomson, A.M. Bannister, A.P. (2003) Interlaminar connections in the neocortex. Cereb. Cortex, 13, 5 14.
57. Vetter, P., Roth, A. Hausser, M. (2001) Propagation of action potentials in dendrites depends on dendritic morphology. J. Neurophysiol., 85, 926 937.
58. Wang, Y., Markram, H., Goodman, P.H., Berger, T.K., Ma, J. Goldman-Rakic, P.S. (2006) Heterogeneity in the pyramidal network of the medial prefrontal cortex. Nat. Neurosci., 9, 534 542.
59. Williams, G.V. Goldman-Rakic, P.S. (1995) Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature, 376, 572 575.
60. Zhou, W.L., Yan, P., Wuskell, J.P., Loew, L.M. Antic, S.D. (2007) Intracellular long wavelength voltage-sensitive dyes for studying the dynamics of action potentials in axons and thin dendrites. J. Neurosci. Meth., 164, 225 239.
61. Zucker, R.S. (1999) Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol., 9, 305 313.