Opinion: An integrated approach to classifying neuronal phenotypes

Nature Reviews Neuroscience

Volumn 6, Issue 10, 2005, Pages 810-818

  Migliore, Michele ^a,b   Shepherd, Gordon M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CNR   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; POTASSIUM CHANNEL; SODIUM CHANNEL; SODIUM ION;

ACTION POTENTIAL; CALCIUM TRANSPORT; CELL ACTIVITY; CELL MEMBRANE DEPOLARIZATION; CELL STRUCTURE; CORRELATION ANALYSIS; DENDRITE; GENE EXPRESSION; GENOTYPE; GOLGI COMPLEX; HUMAN; INTERNEURON; MOLECULAR DYNAMICS; NEOCORTEX; NERVE CELL; NERVE PROJECTION; NONHUMAN; PATCH CLAMP; PHENOTYPE; PRIORITY JOURNAL; PURKINJE CELL; PYRAMIDAL NERVE CELL; REVIEW; SYNAPSE;

ANIMALS; HUMANS; NEURONS; PHENOTYPE;

EID: 27944485730     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn1769     Document Type: Review

References (87)

1. Llinas, R. R. The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242, 1654-1664 (1988).
2. Migliore, M. & Shepherd, G. M. Emerging rules for the distributions of active dendritic conductances. Nature Rev. Neurosci. 3, 362-370 (2002).
3. Toledo-Rodriguez, M. et al. Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb. Cortex 14, 1310-1327 (2004).
4. 2+ signals by small oblique dendrites of CA1 pyramidal neurons. J. Neurosci. 23, 3243-3250 (2003).
5. Stuart, G. & Hausser, M. Initiation and spread of sodium action potentials in cerebellar Purkinje cells. Neuron 13, 703-712 (1994).
6. Williams, S. R. & Stuart, G. J. Action potential backpropagation and somato-dendritic distribution of ion channels in thalamocortical neurons. J. Neurosci. 20, 1307-1317 (2000).
7. Trimmer, J. S. & Rhodes, K. J. Localization of voltagegated ion channels in mammalian brain. Annu. Rev. Physiol. 66, 477-519 (2004).
8. 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).
9. Womack, M. D. & Khodakhah, K. Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J. Neurosci. 24, 3511-3521 (2004).
10. Magee, J. C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J. Neurosci. 18, 7613-7624 (1998).
11. Waters, J., Schaefer, A. & Sakmann, B. Backpropagating action potentials in neurones: measurement, mechanisms and potential functions. Prog. Biophys. Mol. Biol. 87, 145-170 (2005).
12. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387, 869-875 (1997).
13. Stuart, G. J. & Sakmann, B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72 (1994).
14. h in neocortical pyramidal neurons. J. Neurophysiol. 83, 3177-3182 (2000).
15. h channel density in the distal apical dendrite of layer V pyramidal cells increases bidirectional attenuation of EPSPs. J. Neurophysiol. 85, 855-868 (2001).
16. Lorincz, A., Notomi, T., Tamas, G., Shigemoto, R. & Nusser, Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nature Neurosci. 5, 1185-1193 (2002).
17. Hausser, M., Stuart, G., Racca, C. & Sakmann, B. Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15, 637-647 (1995).
18. D'Antuono, M., Biagini, G., Tancredi, V. & Avoli, M. Electrophysiology of regular firing cells in the rat perirhinal cortex. Hippocampus 11, 662-672 (2001).
19. Van der Linden, S. & Lopes da Silva, F. H. Comparison of the electrophysiology and morphology of layers III and II neurons of the rat medial entorhinal cortex in vitro. Eur. J. Neurosci. 10, 1479-1489 (1998).
20. Buckmaster, P. S., Alonso, A., Canfield, D. R. & Amaral, D. G. Dendritic morphology, local circuitry, and intrinsic electrophysiology of principal neurons in the entorhinal cortex of macaque monkeys. J. Comp. Neurol. 470, 317-329 (2004).
21. Protopapas, A. D. & Bower, J. M. Physiological characterization of layer III non-pyramidal neurons in piriform (olfactory) cortex of rat. Brain Res. 865, 1-11 (2000).
22. Cooper, A. J. & Stanford, I. M. Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro. J. Physiol. (Lond.) 527, 291-304 (2000).
23. Kaiser, K. M., Zilberter, Y. & Sakmann, B. Back-propagating action potentials mediate calcium signalling in dendrites of bitufted interneurons in layer 2/3 of rat somatosensory cortex. J. Physiol. (Lond.) 535, 17-31 (2001).
24. + channels in dendritic inhibitory interneurones of rat hippocampus. J. Physiol. (Lond.) 538, 405-419 (2002).
25. Bennett, B. D., Callaway, J. C. & Wilson, C. J. Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J. Neurosci. 20, 8493-8503 (2000).
26. Koizumi, A., Jakobs, T. C. & Masland, R. H. Inward rectifying currents stabilize the membrane potential in dendrites of mouse amacrine cells: patch-clamp recordings and single-cell RT-PCR. Mol. Vis. 10, 328-340 (2004).
27. Bischofberger, J. & Jonas, P. Action potential propagation into the presynaptic dendrites of rat mitral cells. J. Physiol. (Lond.) 504, 359-365 (1997).
28. Holderith, N. B., Shigemoto, R. & Nusser, Z. Cell type-dependent expression of HCN1 in the main olfactory bulb. Eur. J. Neurosci. 18, 344-354 (2003).
29. 2+ influx into dendritic tufts of layer 2/3 neocortical pyramidal neurons in vitro and in vivo. J. Neurosci. 23, 8558-8567 (2003).
30. Maravall, M., Stern, E. A. & Svoboda, K. Development of intrinsic properties and excitability of layer 2/3 pyramidal neurons during a critical period for sensory maps in rat barrel cortex, J. Neurophysiol. 92, 144-156 (2004).
31. Faber, E. S., Callister, R. J. & Sah, P. Morphological and electrophysiological properties of principal neurons in the rat lateral amygdala in vitro. J. Neurophysiol. 85, 714-723 (2001).
32. + conductance in the back-propagation of action potentials in the dendrites of hippocampal neurons. J. Comput. Neurosci. 7, 5-15 (1999).
33. Margrie, T. W., Sakmann, B. & Urban, N. N. Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc. Natl Acad. Sci. USA 98, 319-324 (2001).
34. Stewart, A. E. & Foehring, R. C. Effects of spike parameters and neuromodulators on action potential waveform-induced calcium entry into pyramidal neurons. J. Neurophysiol. 85, 1412-1423 (2001).
35. Magee, J. C. & Johnston, D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213 (1997).
36. Martina, M., Yao, G. L. & Bean, B. P. Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J. Neurosci. 23, 5698-5707 (2003).
37. Velte, T. J. & Masland, R. H. Action potentials in the dendrites of retinal ganglion cells. J. Neurophysiol. 81, 1412-1417 (1999).
38. Buzsaki, G., Penttonen, M., Nadasdy, Z. & Bragin, A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc. Natl Acad. Sci. USA 93, 9921-9925 (1996).
39. Toris, C. B., Eiesland, J. L. & Miller, R. F. Morphology of ganglion cells in the neotenous tiger salamander retina. J. Comp. Neurol. 352, 535-559 (1995).
40. Pinato, G. & Midtgaard, J. Dendritic sodium spikelets and low-threshold calcium spikes in turtle olfactory bulb granule cells. J. Neurophysiol. 93, 1285-1294 (2005).
41. Song, D., Xie, X., Wang, Z. & Berger, T. W. Differential effect of TEA on long-term synaptic modification in hippocampal CA1 and dentate gyrus in vitro. Neurobiol. Learn. Mem. 76, 375-387 (2001).
42. Song, D., Wang, Z. & Berger, T. W. Contribution of T-type VDCC to TEA-induced long-term synaptic modification in hippocampal CA1 and dentate gyrus. Hippocampus 12, 689-697 (2002).
43. H in rat cerebellar Purkinje neurons in vitro. J. Physiol. (Lond.) 539, 469-483 (2002).
44. h normalizes temporal summation in hippocampal CA1 neurons. Nature Neurosci. 2, 508-514 (1999).
45. Migliore, M. On the integration of subthreshold inputs from perforant path and Schaffer collaterals in hippocampal CA1 pyramidal neurons. J. Comput. Neurosci. 14, 185-192 (2003).
46. Henderson, D. & Miller, R. F. Evidence for low-voltage-activated (LVA) calcium currents in the dendrites of tiger salamander retinal ganglion cells. Vis. Neurosci. 20, 141-152 (2003).
47. 2+ current in retinal ganglion cells. J. Neurophysiol. 90, 3888-3901 (2003).
48. Isope, P. & Murphy, T. H. Low threshold calcium currents in rat cerebellar Purkinje cell dendritic spines are mediated by T-type calcium channels. J. Physiol. (Lond.) 562, 257-269 (2005).
49. Usowicz, M. M., Sugimori, M., Cherksey, B. & Llinas, R. P-type calcium channels in the somata and dendrites of adult cerebellar Purkinje cells. Neuron 9, 1185-1199 (1992).
50. McQuiston, A. R. & Katz, L. C. Electro-physiology of interneurons in the glomerular layer of the rat olfactory bulb. J. Neurophysiol. 86, 1899-1907 (2001).
51. Schoppa, N. E. & Westbrook, G. L. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nature Neurosci. 2, 1106-1113 (1999).
52. Egger, V., Svoboda, K. & Mainen, Z. F. Mechanisms of lateral inhibition in the olfactory bulb: efficiency and modulation of spike-evoked calcium influx into granule cells. J. Neurosci. 23, 7551-7558 (2003).
53. Fisher, R. E., Gray, R. & Johnston, D. Properties and distribution of single voltage-gated calcium channels in adult hippocampal neurons. J. Neurophysiol. 64, 91-104 (1990).
54. Buckmaster, P. S. & Amaral, D. G. Intracellular recording and labeling of mossy cells and proximal CA3 pyramidal cells in macaque monkeys. J. Comp. Neurol. 430, 264-281 (2001).
55. h in mouse hippocampal pyramidal neurons. J. Neurosci. 22, 8992-9004 (2002).
56. Golgi, C. Sulle Fina Anatomia Degli Organi Centrali del Sistema Nervoso (Hoepli, Milano, 1886)
57. Ramón y Cajal, S. Histologie du Système Nerveaux de l'Homme et des Vertebres Vol. II (Maloine, Paris, 1911).
58. Ramon-Moliner, E. in The Structure and Function of Nervous Tissue (ed. Bourne, G. H.) 205-267 (Academic, New York, 1968).
59. Kandel, E. R., Schwartz, J. H. & Jessell, T. M. Principles of Neural Science (McGraw-Hill, USA, 2000).
60. Shepherd, G. M. in The Synaptic Organization of the Brain (ed. Shepherd, G. M) 1-38 (Oxford Univ. Press, New York, 2004).
61. Douglas, R., Markram, H. & Martin, K. in The Synaptic Organization of the Brain (ed. Shepherd, G. M.) 499-558 (Oxford Univ. Press, New York, 2004).
62. Rall, W., Shepherd, G. M., Reese, T. S. & Brightman, M. W. Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44-56 (1966).
63. Seamans, J. K. & Yang, C. R. The principal features and mechanisms of dopamine modulation in the prefrontal cortex. Prog. Neurobiol. 74, 1-58 (2004). Erratum: Prog. Neurobiol. 74, 321 (2004).
64. Trudeau, L. E. Glutamate co-transmission as an emerging concept in monoamine neuron function. J. Psychiatry Neurosci. 29, 296-310 (2004).
65. Cherubini, E., Gaiarsa, J. L. & Ben-Ari, Y. GABA: an excitatory transmitter in early postnatal life. Trends Neurosci. 14, 515-519 (1991).
66. Fuxe, K. & Hillarp, N. A. Uptake of L-DOPA and noradrenaline by central catecholamine neurons. Life Sci. 74, 1403-1406 (1964).
67. 2+ current produces input signal amplification and bistability in cat and rat thalamocortical neurones. J. Physiol. (Lond.) 505, 689-705 (1997).
68. Glanzer, J. G. & Eberwine, J. H. Mechanisms of translational control in dendrites. Neurobiol. Aging 24, 1105-1111 (2003).
69. Treloar, H. B., Uboha, U., Jeromin, A. & Greer, C. A. Expression of the neuronal calcium sensor protein NCS-1 in the developing mouse olfactory pathway. J. Comp. Neurol. 482, 201-216 (2005).
70. Stuart, G. & Spruston, N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18, 3501-3510 (1999).
71. Spruston, N. & Johnston, D. Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J. Neurophysiol. 67, 508-529 (1992).
72. Williams, S. R. & Stuart, G. J. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 521, 467-482 (1999).
73. Morin, F., Beaulieu, C. & Lacaille, J. C. Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices. J. Neurophysiol. 76, 1-16 (1996).
74. Bennett, B. D. & Wilson, C. J. Spontaneous activity of neostriatal cholinergic interneurons in vitro. J. Neurosci. 19, 5586-5596 (1999).
75. Manis, P. B. Membrane properties and discharge characteristics of guinea pig dorsal cochlear nucleus neurons studied in vitro. J. Neurosci. 10, 2338-2351 (1990).
76. Chen, W. R. & Shepherd, G. M. Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res. 745, 189-196 (1997).
77. Mason, A. & Larkman, A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J. Neurosci. 10, 1415-1428 (1990).
78. Kroner, S., Gottmann, K., Hatt, H. & Gunturkun, O. Electrophysiological and morphological properties of cell types in the chick neostriatum caudolaterale. Neuroscience 110, 459-473 (2002).
79. h modulation of burst firing and δ oscillations in thalamocortical neurons in vitro. Neuroscience 87, 541-550 (1998).
80. Swensen, A. M. & Bean, B. P. Ionic mechanisms of burst firing in dissociated Purkinje neurons. J. Neurosci. 23, 9650-9663 (2003).
81. Chang, W., Strahlendorf, J. C. & Strahlendorf, H. K. Ionic contributions to the oscillatory firing activity of rat Purkinje cells in vitro. Brain Res. 614, 335-341 (1993).
82. Sheasby, B. W. & Fohlmeister, J. F. Impulse encoding across the dendritic morphologies of retinal ganglion cells. J. Neurophysiol. 81, 1685-1698 (1999).
83. Tabata, T. & Ishida, A. T. Transient and sustained depolarization of retinal ganglion cells by Ih. J. Neurophysiol. 75, 1932-1943 (1996).
84. 2+ transients evoked by action potentials in rat dorsal cochlear nucleus pyramidal and cartwheel neurons. J. Neurophysiol. 89, 2225-2237 (2003).
85. Manis, P. B., Spirou, G. A., Wright, D. D., Paydar, S. & Ryugo, D. K. Physiology and morphology of complex spiking neurons in the guinea pig dorsal cochlear nucleus. J. Comp. Neurol. 348, 261-276 (1994).
86. +-dependent mechanism. J. Neurosci. 21, 759-770 (2001).
87. St. John, J. L., Rosene, D. L. & Luebke, J. I. Morphology and electrophysiology of dentate granule cells in the rhesus monkey: comparison with the rat. J. Comp. Neurol. 387, 136-147 (1997).