Dendrite-to-soma input/output function of continuous time-varying signals in hippocampal CA1 pyramidal neurons

Journal of Neurophysiology

Volumn 98, Issue 5, 2007, Pages 2943-2955

  Cook, Erik P ^a   Guest, Jennifer A ^b   Liang, Yong ^b   Masse, Nicolas Y ^a   Colbert, Costa M ^b  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF HOUSTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENDRITIC CELL; DYNAMICS; FREQUENCY ANALYSIS; HIPPOCAMPUS; IN VIVO STUDY; MALE; MEMBRANE POTENTIAL; NERVE CELL MEMBRANE POTENTIAL; NEUROPHYSIOLOGY; NONHUMAN; NONLINEAR SYSTEM; PERCEPTIVE THRESHOLD; PERIKARYON; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SIGNAL TRANSDUCTION; SOMATIC CELL; STATISTICS; VARIANCE; WHOLE CELL;

ACTION POTENTIALS; ANIMALS; AXONS; DENDRITES; DOSE-RESPONSE RELATIONSHIP, RADIATION; ELECTRIC STIMULATION; HIPPOCAMPUS; MALE; MODELS, NEUROLOGICAL; PATCH-CLAMP TECHNIQUES; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

EID: 36248932610     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00414.2007     Document Type: Article

References (117)

1. Albrecht DG, Farrar SB, Hamilton DB. Spatial contrast adaptation characteristics of neurons recorded in the cat's visual cortex. J Physiol 347: 713-739, 1984.
2. Anderson JS, Lampl I, Gillespie DC, Ferster D. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290: 1968-1972, 2000.
3. Ariav G, Polsky A, Schiller J. Submillisecond precision of the input-output transformation function mediated by fast sodium dendritic spikes in basal dendrites of CA1 pyramidal neurons. J Neurosci 23: 7750-7758, 2003.
4. Atick JJ. Could information theory provide an ecological theory of sensory processing? Network 3: 213-251, 1992.
5. Azouz R. Dynamic spatiotemporal synaptic integration in cortical neurons: neuronal gain, revisited. J Neurophysiol 94: 2785-2796, 2005.
6. Baccus SA, Meister M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36: 909-919, 2002.
7. Barlow HB. Possible principles underlying the transformation of sensory messages. In: Sensory Communication, edited by RosenBlith WA. Cambridge, MA: MIT Press, 1961, p. 217-234.
8. Bialek W, Rieke F. Reliability and information transmission in spiking neurons. Trends Neurosci 15: 428-434, 1992.
9. Binder MD, Poliakov AV, Powers RK. Functional identification of the input-output transforms of mammalian motoneurones. J Physiol 93: 29-42, 1999.
10. Borg-Graham LJ, Monier C, Fregnac Y. Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393: 369-373, 1998.
11. Britten KH, Newsome WT, Shadlen MN, Celebrini S, Movshon JA. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis Neurosci 13: 87-100, 1996.
12. Bryant HL, Segundo JP. Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260: 279-314, 1976.
13. Burdakov D. Gain control by concerted changes in I(A) and I(H) conductances. Neural Comput 17: 991-995, 2005.
14. Buzsaki G. Theta oscillations in the hippocampus. Neuron 33: 325-340, 2002.
15. Carandini M, Heeger DJ. Summation and division by neurons in primate visual cortex. Science 264: 1333-1336, 1994.
16. Cash S, Yuste R. Linear summation of excitatory inputs by CA1 pyramidal neurons. Neuron 22: 383-394, 1999.
17. Chance FS, Abbott LF, Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
18. Chichilnisky EJ. A simple white noise analysis of neuronal light responses. Network 12: 199-213, 2001.
19. Colbert CM, Pan E. Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5: 533-538, 2002.
20. Cook EP, Guest JA, Colbert CM. White-noise analysis of CA1 pyramidal dendrites reveals linear signal processing with boosting of subthreshold inputs. Soc Neurosci Abstr 738.3, 2005.
21. Cook EP, Maunsell JHR. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat Neurosci 5: 985-994, 2002a.
22. Cook EP, Maunsell JHR. Attentional modulation of behavioral performance and neuronal responses in Middle Temporal and Ventral Intraparietal areas of macaque monkey. J Neurosci 22: 1994-2004, 2002b.
23. Cook EP, Maunsell JH. Attentional modulation of motion integration of individual neurons in the middle temporal visual area. J Neurosci 24: 7964-7977, 2004.
24. Davis GW, Bezprozvanny I. Maintaining the stability of neural function: a homeostatic hypothesis. Annu Rev Physiol 63: 847-869, 2001.
25. Destexhe A, Pare D. Impact of network activity on the integrative properties of neocortical pyramidal neurons in vivo. J Neurophysiol 81: 1531-1547, 1999.
26. Destexhe A, Rudolph M, Pare D. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751, 2003.
27. Dodd JV, Krug K, Cumming BG, Parker AJ. Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J Neurosci 21: 4809-4821, 2001.
28. Efron B, Tibshirani R. An Introduction to the Bootstrap. London: Chapman and Hall, 1993.
29. Erchova I, Kreck G, Heinemann U, Herz AV. Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold. J Physiol 560: 89-110, 2004.
30. Fairhall AL, Lewen GD, Bialek W, de Ruyter Van Steveninck RR. Efficiency and ambiguity in an adaptive neural code. Nature 412: 787-792, 2001.
31. Ferster D, Jagadeesh B. EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J Neurosci 12: 1262-1274, 1992.
32. Gasparini S, Magee JC. State-dependent dendritic computation in hippocampal CA1 pyramidal neurons. J Neurosci 26: 2088-2100, 2006.
33. Gasparini S, Migliore M, Magee JC. On the initiation and propagation of dendritic spikes in CA1 pyramidal neurons. J Neurosci 24: 11046-11056, 2004.
34. Golding NL, Spruston N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21: 1189-1200, 1998.
35. Hausser M, Mel B. Dendrites: bug or feature? Curr Opin Neurobiol 13: 372-383, 2003.
36. Hausser M, Spruston N, Stuart GJ. Diversity and dynamics of dendritic signaling. Science 290: 739-744, 2000.
37. Higgs MH, Slee SJ, Spain WJ. Diversity of gain modulation by noise in neocortical neurons: regulation by the slow afterhyperpolarization conductance. J Neurosci 26: 8787-8799, 2006.
38. Hirsch JA, Alonso JM, Reid RC, Martinez LM. Synaptic integration in striate cortical simple cells. J Neurosci 18: 9517-9528, 1998.
39. Ho N, Destexhe A. Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J Neurophysiol 84: 1488-1496, 2000.
40. Holt GR, Koch C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9: 1001-1013, 1997.
41. Hosoya T, Baccus SA, Meister M. Dynamic predictive coding by the retina. Nature 436: 71-77, 2005.
42. Hunter IW, Korenberg MJ. The identification of nonlinear biological systems: Wiener and Hammerstein cascade models. Biol Cybern 55: 135-144, 1986.
43. Hutcheon B, Miura RM, Puil E. Subthreshold membrane resonance in neocortical neurons. J Neurophysiol 76: 683-697, 1996.
44. Hutcheon B, Yarom Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23: 216-222, 2000.
45. Ishizuka N, Cowan WM, Amaral DG. A quantitative analysis of the dendritic organization of pyramidal cells in the rat hippocampus. J Comp Neurol 362: 17-45, 1995.
46. Jahnsen H, Karnup S. A spectral analysis of the integration of artificial synaptic potentials in mammalian central neurons. Brain Res 666: 9-20, 1994.
47. Johnston D, Magee JC, Colbert CM, Cristie BR. Active properties of neuronal dendrites. Annu Rev Neurosci 19: 165-186, 1996.
48. Jones JP, Palmer LA. The two-dimensional spatial structure of simple receptive fields in cat striate cortex. J Neurophysiol 58: 1187-1211, 1987.
49. Kamondi A, Acsady L, Buzsaki G. Dendritic spikes are enhanced by cooperative network activity in the intact hippocampus. J Neurosci 18: 3919-3928, 1998.
50. Kerr AM, Capogna M. Unitary IPSPs enhance hilar mossy cell gain in the rat hippocampus. J Physiol 578: 451-470, 2007.
51. Kim KJ, Rieke F. Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J Neurosci 21: 287-299, 2001.
52. Korenberg MJ, French AS, Voo SK. White-noise analysis of nonlinear behavior in an insect sensory neuron: kernel and cascade approaches. Biol Cybern 58: 313-320, 1988.
53. Korenberg MJ, Sakai HM, Naka K. Dissection of the neuron network in the catfish inner retina. III. Interpretation of spike kernels. J Neurophysiol 61: 1110-1120, 1989.
54. Larkum ME, Senn W, Luscher HR. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb Cortex 14: 1059 -1070, 2004.
55. + action potentials in distal and terminal dendrites of rat neocortical pyramidal neurons in vitro and in vivo. J Neurosci 22: 6991-7005, 2002.
56. Larkum ME, Zhu JJ, Sakmann B. Dendritic mechanisms underlying the coupling of the dendritic with the axonal action potential initiation zone of adult rat layer 5 pyramidal neurons. J Physiol 533: 447-466, 2001.
57. Lengyel M, Huhn Z, Erdi P. Computational theories on the function of theta oscillations. Biol Cybern 92: 393-408, 2005.
58. Leung LS, Yu HW. Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J Neurophysiol 79: 1592-1596, 1998.
59. London M, Hausser M. Dendritic computation. Annu Rev Neurosci 28: 503-532, 2005.
60. Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci 5: 1185-1193, 2002.
61. Maffei L, Fiorentini A, Bisti S. Neural correlate of perceptual adaptation to gratings. Science 182: 1036-1038, 1973.
62. Magee JC. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. J Neurosci 18: 7613-7624, 1998.
63. Magee JC. Dendritic lh normalizes temporal summation in hippocampal CA1 neurons. Nat Neurosci 2: 508-514, 1999.
64. Magee JC. Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1: 181-190, 2000.
65. Magee JC, Johnston D. Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268: 301-304, 1995.
66. Magee JC, Johnston D. Plasticity of dendritic function. Curr Opin Neurobiol 15: 334-342, 2005.
67. Mainen ZF, Sejnowski TJ. Reliability of spike timing in neocortical neurons. Science 268: 1503-1506, 1995.
68. Markus EJ, Qin YL, Leonard B, Skaggs WE, McNaughton BL, Barnes CA. Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079-7094, 1995.
69. Marmarelis PZ, Marmarelis VZ. Analysis of Physiological Systems: The White Noise Approach. New York: Plenum, 1978.
70. McAdams CJ, Maunsell JHR. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area V4. J Neurosci 19: 431-441, 1999.
71. Meister M, Berry MJ Jr. The neural code of the retina. Neuron 22: 435-450, 1999.
72. Mel BW. Synaptic integration in an excitable dendritic tree. J Neurophysiol 70: 1086-1101, 1993.
73. Migliore M, Shepherd GM. Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3: 362-370, 2002.
74. Mitchell SJ, Silver RA. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38: 433-445, 2003.
75. Moore LE, Christensen BN. White noise analysis of cable properties of neuroblastoma cells and lamprey central neurons. J Neurophysiol 53: 636-651, 1985.
76. Movshon JA, Lennie P. Pattern-selective adaptation in visual cortical neurones. Nature 278: 850-852, 1979.
77. Nettleton JS, Spain WJ. Linear to supralinear summation of AMPA-mediated EPSPs in neocortical pyramidal neurons. J Neurophysiol 83: 3310-3322, 2000.
78. Nevian T, Larkum ME, Polsky A, Schiller J. Properties of basal dendrites of layer 5 pyramidal neurons: a direct patch-clamp recording study. Nat Neurosci 10: 206-214, 2007.
79. Oviedo H, Reyes AD. Boosting of neuronal firing evoked with asynchronous and synchronous inputs to the dendrite. Nat Neurosci 5: 261-266, 2002.
80. Oviedo H, Reyes AD. Variation of input-output properties along the somatodendritic axis of pyramidal neurons. J Neurosci 25: 4985-4995, 2005.
81. Poliakov AV, Powers RK, Binder MD. Functional identification of the input-output transforms of motoneurons in the rat and cat. J Physiol 504: 401-424, 1997.
82. Polsky A, Mel BW, Schiller J. Computational subunits in thin dendrites of pyramidal cells. Nat Neurosci 7: 621-627, 2004.
83. Prescott SA, De Koninck Y. Gain control of firing rate by shunting inhibition: roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci USA 100: 2076-2081, 2003.
84. Purushothaman G, Bradley DC. Neural population code for fine perceptual decisions in area MT. Nat Neurosci 8: 99-106, 2005.
85. Rall W. Branching dendritic trees and motoneuron membrane resistivity. Exp Neurol 1: 491-527, 1959.
86. Rauch A, La Camera G, Luscher HR, Senn W, Fusi S. Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. J Neurophysiol 90: 1598-1612, 2003.
87. Reyes A. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24: 653-675, 2001.
88. Reynolds JH, Pasternak T, Desimone R. Attention increases sensitivity of V4 neurons. Neuron 26: 703-714, 2000.
89. Sakai HM. White-noise analysis in neurophysiology. Physiol Rev 72: 491-505, 1992.
90. Salinas E, Abbott LF. Invariant visual responses from attentional gain fields. J Neurophysiol 77: 3267-3272, 1997.
91. Salinas E, Sejnowski TJ. Gain modulation in the central nervous system: where behavior, neurophysiology, and computation meet. Neuroscientist 7: 430-440, 2001.
92. Salinas E, Thier P. Gain modulation: a major computational principle of the central nervous system. Neuron 27: 15-21, 2000.
93. Sanchez-Vives MV, Nowak LG, McCormick DA. Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20: 4267-4285, 2000.
94. Schaefer AT, Larkum ME, Sakmann B, Roth A. Coincidence detection in pyramidal neurons is tuned by their dendritic branching pattern. J Neurophysiol 89: 3143-3154, 2003.
95. Schwindt PC, Crill WE. Local and propagated dendritic action potentials evoked by glutamate iontophoresis on rat neocortical pyramidal neurons. J Neurophysiol 77: 2466-2483, 1997.
96. Segev I, London M. Untangling dendrites with quantitative models. Science 290: 744-750, 2000.
97. Shu Y, Hasenstaub A, Badoual M, Bal T, McCormick DA. Barrages of synaptic activity control the gain and sensitivity of cortical neurons. J Neurosci 23: 10388-10401, 2003.
98. Slee SJ, Higgs MH, Fairhall AL, Spain WJ. Two-dimensional time coding in the auditory brain stem. J Neurosci 25: 9978-9988, 2005.
99. Stein RB, Gossen ER, Jones KE. Neuronal variability: noise or part of the signal? Nat Rev Neurosci 6: 389-397, 2005.
100. Stuart G, Schiller J, Sakmann B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J Physiol 505: 617-632, 1997.
101. Tamas G, Szabadics J, Somogyi P. Cell type- and subcellular position-dependent summation of unitary postsynaptic potentials in neocortical neurons. J Neurosci 22: 740-747, 2002.
102. Treue S, Martinez Trujillo JC. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399: 575-579, 1999.
103. Turner RW, Meyers DE, Richardson TL, Barker JL. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. J Neurosci 11: 2270-2280, 1991.
104. Turrigiano GG, Nelson SB. Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10: 358-364, 2000.
105. Uka T, DeAngelis GC. Contribution of area MT to stereoscopic depth perception: choice-related response modulations reflect task strategy. Neuron 42: 297-310, 2004.
106. Ulrich D. Dendritic resonance in rat neocortical pyramidal cells. J Neurophysiol 87: 2753-2759, 2002.
107. Urban NN, Barrionuevo G. Active summation of excitatory postsynaptic potentials in hippocampal CA3 pyramidal neurons. Proc Natl Acad Sci USA 95: 11450-11455, 1998.
108. Van Wezel RJ, Britten KH. Motion adaptation in area MT. J Neurophysiol 88: 3469-3476, 2002.
109. Wei DS, Mei YA, Bagal A, Kao JP, Thompson SM, Tang CM. Compartmentalized and binary behavior of terminal dendrites in hippocampal pyramidal neurons. Science 293: 2272-2275, 2001.
110. Westwick DT Kearney RE. Identification of Nonlinear Physiological Systems. Piscataway: IEEE Press, 2003.
111. Williams SR. Spatial compartmentalization and functional impact of conductance in pyramidal neurons. Nat Neurosci 7: 961-967, 2004.
112. Williams SR, Stuart GJ. Site independence of EPSP time course is mediated by dendritic I(h) in neocortical pyramidal neurons. J Neurophysiol 83: 3177-3182, 2000.
113. Williams SR, Stuart GJ. Dependence of EPSP efficacy on synapse location in neocortical pyramidal neurons. Science 295: 1907-1910, 2002.
114. Womack MD, Khodakhah K. Dendritic control of spontaneous bursting in cerebellar Purkinje cells. J Neurosci 24: 3511-3521, 2004.
115. Wright WN, Bardakjian BL, Valiante TA, Perez-Velazquez JL, Carlen PL. White noise approach for estimating the passive electrical properties of neurons. J Neurophysiol 76: 3442-3450, 1996.
116. Wu MC, David SV, Gallant JL. Complete functional characterization of sensory neurons by system identification. Annu Rev Neurosci 29: 477-505, 2006.
117. Yoganarasimha D, Yu X, Knierim JJ. Head direction cell representations maintain internal coherence during conflicting proximal and distal cue rotations: comparison with hippocampal place cells. J Neurosci 26: 622-631, 2006.