Differential behavioral state-dependence in the burst properties of CA3 and CA1 neurons

Neuroscience

Volumn 141, Issue 4, 2006, Pages 1665-1677

  Tropp Sneider, J ^a,b   Chrobak, J J ^a   Quirk, M C ^c   Oler, J A ^a,d   Markus, E J ^a  

^a UNIVERSITY OF CONNECTICUT   (United States)

^b MCLEAN HOSPITAL   (United States)

^c Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

epilepsy; hippocampus; learning; place cell; plasticity; theta

Indexed keywords

ACTION POTENTIAL; AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENUATION; BEHAVIOR CHANGE; BRAIN REGION; CONTROLLED STUDY; FEMALE; IMMOBILIZATION; IN VIVO STUDY; MATHEMATICAL MODEL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; RUNNING; TASK PERFORMANCE; WAKEFULNESS;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; FEMALE; HIPPOCAMPUS; IMMOBILITY RESPONSE, TONIC; MAZE LEARNING; MODELS, NEUROLOGICAL; PYRAMIDAL CELLS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33747173006     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2006.05.052     Document Type: Article

References (71)

1. Azouz R., Jensen M.S., and Yaari Y. Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol 492 Pt 1 (1996) 211-223
2. Bernard C., and Johnston D. Distance-dependent modifiable threshold for action potential back-propagation in hippocampal dendrites. J Neurophysiol 90 (2003) 1807-1816
3. Buzsáki G. Two-stage model of memory trace formation. a role for "noisy" brain states. Neuroscience 31 (1989) 551-570
4. Buzsáki G., Penttonen M., Nadasdy Z., and Bragin A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc Natl Acad Sci U S A 93 (1996) 9921-9925
5. Buzsáki G., Csicsvari J., Dragoi G., Harris K., Henze D., and Hirase H. Homeostatic maintenance of neuronal excitability by burst discharges in vivo. Cereb Cortex 12 (2002) 893-899
6. Chrobak J.J., and Buzsáki G. Operational dynamics in the hippocampal-entorhinal axis. Neurosci Biobehav Rev 22 (1998) 303-310
7. Claiborne B.J., Amaral D.G., and Cowan W.M. A light and electron microscopic analysis of the mossy fibers of the rat dentate gyrus. J Comp Neurol 246 (1986) 435-458
8. Cohen N.J., and Eichenbaum H. Memory, amnesia, and the hippocampal system (1993), MIT Press, Cambridge
9. Connors B.W., and Gutnick M.J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 13 (1990) 99-104
10. Cousens G., and Otto T.A. Induction and transient suppression of long-term potentiation in the peri- and postrhinal cortices following theta-related stimulation of hippocampal field CA1. Brain Res 780 (1998) 95-101
11. Csicsvari J., Hirase H., Mamiya A., and Buzsáki G. Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28 (2000) 585-594
12. Guzowski J.F., Knierim J.J., and Moser E.I. Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 44 (2004) 581-584
13. Harris K.D., Hirase H., Leinekugel X., Henze D.A., and Buzsáki G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32 (2001) 141-149
14. Harris K.D., Henze D.A., Hirase H., Leinekugel X., Dragoi G., Czurko A., and Buzsáki G. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417 (2002) 738-741
15. Hasselmo M.E., and Bower J.M. Acetylcholine and memory. Trends Neurosci 16 (1993) 218-222
16. Hasselmo M.E., and Schnell E. Laminar selectivity of the cholinergic suppression of synaptic transmission in rat hippocampal region CA1. computational modeling and brain slice physiology. J Neurosci 14 (1994) 3898-3914
17. Hasselmo M.E., Schnell E., and Barkai E. Dynamics of learning and recall at excitatory recurrent synapses and cholinergic modulation in rat hippocampal region CA3. J Neurosci 15 (1995) 5249-5262
18. Hasselmo M.E., Wyble B.P., and Wallenstein G.V. Encoding and retrieval of episodic memories. role of cholinergic and GABAergic modulation in the hippocampus. Hippocampus 6 (1996) 693-708
19. Hirase H., Leinekugel X., Czurko A., Csicsvari J., and Buzsáki G. Firing rates of hippocampal neurons are preserved during subsequent sleep episodes and modified by novel awake experience. Proc Natl Acad Sci U S A 98 16 (2001) 9386-9390
20. Huguenard J.R. Low-threshold calcium currents in central nervous system neurons. Annu Rev Physiol 58 (1996) 329-348
21. Kandel E.R., and Spencer W.A. Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol 24 (1961) 243-259
22. Kepecs A., Wang X.J., and Lisman J. Bursting neurons signal input slope. J Neurosci 22 (2002) 9053-9062
23. Klausberger T., Magill P.J., Marton L.F., Roberts J.D., Cobden P.M., Buzsáki G., and Somogyi P. Brain-state- and cell-type-specific firing of hippocampal interneurons in vivo. Nature 421 (2003) 844-848
24. Kloosterman F., Van Haeften T., Witter M.P., and Lopes Da Silva F.H. Electrophysiological characterization of interlaminar entorhinal connections. an essential link for re-entrance in the hippocampal-entorhinal system. Eur J Neurosci 18 (2003) 3037-3052
25. Kudrimoti H.S., Barnes C.A., and McNaughton B.L. Reactivation of hippocampal cell assemblies. effects of behavioral state, experience, and EEG dynamics. J Neurosci 19 (1999) 4090-4101
26. Lee A.K., and Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36 (2002) 1183-1194
27. Lee I., and Kesner R.P. Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nat Neurosci 5 (2002) 162-168
28. Lee I., Rao G., and Knierim J.J. A double dissociation between hippocampal subfields. differential time course of CA3 and CA1 place cells for processing changed environments. Neuron 42 (2004) 803-815
29. Lee I., Yoganarasimha D., Rao G., and Knierim J.J. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430 (2004) 456-459
30. Leutgeb S., Leutgeb J.K., Treves A., Moser M.B., and Moser E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305 (2004) 1295-1298
31. Lisman J.E. Bursts as a unit of neural information. making unreliable synapses reliable. Trends Neurosci 20 (1997) 38-43
32. Lisman J.E., and Otmakhova N.A. Storage, recall, and novelty detection of sequences by the hippocampus. elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11 (2001) 551-568
33. Llinas R.R. The intrinsic electrophysiological properties of mammalian neurons. insights into central nervous system function. Science 242 (1988) 1654-1664
34. Magee J.C., and Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275 (1997) 209-213
35. Markus E.J., Barnes C.A., McNaughton B.L., Gladden V., and Skaggs W.E. Spatial information content and reliability of hippocampal CA1 neurons. Effects of visual input. Hippocampus 4 (1994) 410-421
36. McNaughton B.L., and Morris R.G.M. Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10 (1987) 408-415
37. McNaughton B.L., Barnes C.A., Meltzer J., and Sutherland R.J. Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp Brain Res 76 (1989) 485-496
38. Metzner W., Koch C., Wessel R., and Gabbiani F. Feature extraction by burst-like spike patterns in multiple sensory maps. J Neurosci 18 (1998) 2283-2300
39. Mizumori S.J.Y., McNaughton B.L., and Barnes C.A. A comparison of supramammillary and medial septal influences on hippocampal field potentials and single-unit activity. J Neurophysiol 7 (1989) 15-31
40. Nadasdy Z., Hirase H., Czurko A., Csicsvari J., and Buzsáki G. Replay and time compression of recurring spike sequences in the hippocampus. J Neurosci 19 (1999) 9497-9507
41. Nitz D., and McNaughton B. Differential modulation of CA1 and dentate gyrus interneurons during exploration of novel environments. J Neurophysiol 91 (2004) 863-872
42. Nitz D.A., and McNaughton B.L. Hippocampal EEG and unit activity responses to modulation of serotonergic median raphe neurons in the freely behaving rat. Learn Mem 6 (1999) 153-167
43. O'Keefe J., and Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34 (1971) 171-175
44. O'Keefe J., and Nadel L. The hippocampus as a cognitive map (1978), Clarendon Press, Oxford
45. O'Keefe J., and Recce M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3 (1993) 317-330
46. Oler J.A., and Markus E.J. Age related deficits in the ability to encode contextual change. a place cell analysis. Hippocampus 10 (2000) 338-350
47. Otto T., Eichenbaum H., Wiener S.I., and Wible C.G. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1 (1991) 181-192
48. Pike F.G., Meredith R.M., Olding A.W., and Paulsen O. Rapid report. postsynaptic bursting is essential for "Hebbian" induction of associative long-term potentiation at excitatory synapses in rat hippocampus. J Physiol 518 Pt 2 (1999) 571-576
49. Quirk M.C., and Wilson M.A. Interaction between spike waveform classification and temporal sequence detection. J Neurosci Methods 94 (1999) 41-52
50. Quirk M.C., Blum K.I., and Wilson M.A. Experience-dependent changes in extracellular spike amplitude may reflect regulation of dendritic action potential back-propagation in rat hippocampal pyramidal cells. J Neurosci 21 (2001) 240-248
51. Ranck J.B.J. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol 41 (1973) 461-531
52. Reinagel P., Godwin D., Sherman S.M., and Koch C. Encoding of visual information by LGN bursts. J Neurophysiol 81 (1999) 2558-2569
53. Scharfman H.E., and MacLusky N.J. Similarities between actions of estrogen and BDNF in the hippocampus. coincidence or clue?. Trends Neurosci 28 (2005) 79-85
54. Schwindt P., and Crill W. Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. J Neurophysiol 81 (1999) 1341-1354
55. Scoville W.B., and Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20 (1957) 11-21
56. Staff N.P., Jung H.Y., Thiagarajan T., Yao M., and Spruston N. Resting and active properties of pyramidal neurons in subiculum and CA1 of rat hippocampus. J Neurophysiol 84 (2000) 2398-2408
57. Steward O., and Scoville S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentate of the rat. J Comp Neurol 169 (1976) 347-370
58. Sutherland R.J., and Rudy J.W. Configural association theory. The role of the hippocampal formation in learning, memory, and amnesia. Psychobiology 17 (1989) 129-144
59. Swadlow H.A., and Gusev A.G. The impact of "bursting" thalamic impulses at a neocortical synapse. Nat Neurosci 4 (2001) 402-408
60. Tamamaki N., and Nojyo Y. Projection of the entorhinal layer II neurons in the rat as revealed by intracellular pressure-injection of neurobiotin. Hippocampus 3 (1993) 471-480
61. Thompson S.M. Synaptic plasticity. Building memories to last. Curr Biol 10 (2000) R218-R221
62. Traub R.D., Wong R.K., Miles R., and Michelson H. A model of a CA3 hippocampal pyramidal neuron incorporating voltage-clamp data on intrinsic conductances. J Neurophysiol 66 (1991) 635-650
63. Tropp J., and Markus E.J. Effects of mild food deprivation on the estrous cycle of rats. Physiol Behav 73 (2001) 553-559
64. Tropp J., Figueiredo C.M., and Markus E.J. Stability of hippocampal place cell activity across the rat estrous cycle. Hippocampus 15 (2005) 154-165
65. van Groen T., and Wyss J.M. Extrinsic projections from area CA1 of the rat hippocampus. olfactory, cortical, subcortical, and bilateral hippocampal formation projections. J Comp Neurol 302 (1990) 515-528
66. Vargha-Khadem F., Gadian D.G., Watkins K.E., Connelly A., Van Paesschen W., and Mishkin M. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277 (1997) 376-380
67. Williams S.R., and Stuart G.J. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521 Pt 2 (1999) 467-482
68. Wilson M.A., and McNaughton B.L. Dynamics of the hippocampal ensemble code for space. Science 261 (1993) 1055-1058
69. Wilson M.A., and McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 265 (1994) 676-679
70. Wong R.K., and Prince D.A. Participation of calcium spikes during intrinsic burst firing in hippocampal neurons. Brain Res 159 (1978) 385-390
71. Wong R.K., and Stewart M. Different firing patterns generated in dendrites and somata of CA1 pyramidal neurons in guinea-pig hippocampus. J Physiol 457 (1992) 675-687