 |
Previous Article | Next Article 
Volume 16, Number 9,
Issue of May 1, 1996
pp. 3056-3066
Copyright ©1996 Society for Neuroscience
High-Frequency Oscillations in the Output Networks of the
Hippocampal-Entorhinal Axis of the Freely Behaving Rat
Received Nov. 30, 1995; revised Jan. 18, 1996; accepted Jan. 22, 1996.
James J. Chrobak and
Gyorgy Buzsáki
Center for Molecular and Behavioral Neuroscience, Rutgers, The
State University of New Jersey, Newark, New Jersey 07102
Population bursts of the CA3 network, which occur during eating,
drinking, awake immobility, and slow-wave sleep, produce a large field
excitatory postsynaptic potential throughout stratum radiatum of the
CA1 field (sharp wave). The CA3 burst sets into motion a short-lived,
dynamic interaction between CA1 pyramidal cells and interneurons, the
product of which is a 200 Hz oscillatory field potential (ripple) and
phase-related discharge of the CA1 network. Although many CA1 pyramidal
neurons discharge during the time frame (50-100 msec) of each sharp
wave, each wave of a ripple (~5 msec) reflects the synchronization of
more discrete subsets of CA1 neurons.
When we used multi-site recordings in freely behaving rats, we observed
ripples throughout the longitudinal extent (~4-5 mm) of the dorsal
CA1 region that were coherent for multiple cycles of each ripple.
High-frequency ripples were also observed throughout the
hippocampal-entorhinal output pathway that were concurrent but less
coherent on a cycle-by-cycle basis. Single and multiunit neuronal
activity was phase-related to local ripples throughout the
hippocampal-entorhinal output pathway. Entorhinal ripples occurred
5-30 msec after the CA1 ripples and were related to the occurrence of
an entorhinal sharp wave. Thus, during each hippocampal sharp wave,
there is a powerful synchronization among the neuronal networks that
connect the hippocampus to the neocortex. We suggest that this
population interaction (1) biologically constrains theoretical models
of hippocampal function and dysfunction and (2) has the capacity to
support an ``off-line'' memory consolidation process.
Key words:
hippocampus;
subiculum;
entorhinal cortex;
oscillations;
sharp waves;
memory;
epilepsy
This article has been cited by other articles:

|
 |

|
 |
 
M. J. Jutras, P. Fries, and E. A. Buffalo
Gamma-Band Synchronization in the Macaque Hippocampus and Memory Formation
J. Neurosci.,
October 7, 2009;
29(40):
12521 - 12531.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. C. Stacey, M. T. Lazarewicz, and B. Litt
Synaptic Noise and Physiological Coupling Generate High-Frequency Oscillations in a Hippocampal Computational Model
J Neurophysiol,
October 1, 2009;
102(4):
2342 - 2357.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Jacobs, P. LeVan, C.-E. Chatillon, A. Olivier, F. Dubeau, and J. Gotman
High frequency oscillations in intracranial EEGs mark epileptogenicity rather than lesion type
Brain,
April 1, 2009;
132(4):
1022 - 1037.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. Martuzzi, M. M. Murray, R. A. Meuli, J.-P. Thiran, P. P. Maeder, C. M. Michel, R. Grave de Peralta Menendez, and S. L. Gonzalez Andino
Methods for Determining Frequency- and Region-Dependent Relationships Between Estimated LFPs and BOLD Responses in Humans
J Neurophysiol,
January 1, 2009;
101(1):
491 - 502.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Axmacher, C. E. Elger, and J. Fell
Ripples in the medial temporal lobe are relevant for human memory consolidation
Brain,
July 1, 2008;
131(7):
1806 - 1817.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Le Van Quyen, A. Bragin, R. Staba, B. Crepon, C. L. Wilson, and J. Engel Jr
Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans
J. Neurosci.,
June 11, 2008;
28(24):
6104 - 6110.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Worrell, A. B. Gardner, S. M. Stead, S. Hu, S. Goerss, G. J. Cascino, F. B. Meyer, R. Marsh, and B. Litt
High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macroelectrode recordings
Brain,
April 1, 2008;
131(4):
928 - 937.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Sava and E. J. Markus
Activation of the Medial Septum Reverses Age-Related Hippocampal Encoding Deficits: A Place Field Analysis
J. Neurosci.,
February 20, 2008;
28(8):
1841 - 1853.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Urrestarazu, R. Chander, F. Dubeau, and J. Gotman
Interictal high-frequency oscillations (100 500 Hz) in the intracerebral EEG of epileptic patients
Brain,
September 1, 2007;
130(9):
2354 - 2366.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Jinno, T. Klausberger, L. F. Marton, Y. Dalezios, J. D. B. Roberts, P. Fuentealba, E. A. Bushong, D. Henze, G. Buzsaki, and P. Somogyi
Neuronal Diversity in GABAergic Long-Range Projections from the Hippocampus
J. Neurosci.,
August 15, 2007;
27(33):
8790 - 8804.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. E. Skaggs, B. L. McNaughton, M. Permenter, M. Archibeque, J. Vogt, D. G. Amaral, and C. A. Barnes
EEG Sharp Waves and Sparse Ensemble Unit Activity in the Macaque Hippocampus
J Neurophysiol,
August 1, 2007;
98(2):
898 - 910.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Axmacher, F. Mormann, G. Fernandez, M. X Cohen, C. E. Elger, and J. Fell
Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe
J. Neurosci.,
July 18, 2007;
27(29):
7807 - 7816.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Jackson, A. Johnson, and A. D. Redish
Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience
J. Neurosci.,
November 29, 2006;
26(48):
12415 - 12426.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Born, B. Rasch, and S. Gais
Sleep to Remember
Neuroscientist,
October 1, 2006;
12(5):
410 - 424.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
C. Schmidt, P. Peigneux, V. Muto, M. Schenkel, V. Knoblauch, M. Munch, D. J.-F. de Quervain, A. Wirz-Justice, and C. Cajochen
Encoding Difficulty Promotes Postlearning Changes in Sleep Spindle Activity during Napping.
J. Neurosci.,
August 30, 2006;
26(35):
8976 - 8982.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Molle, O. Yeshenko, L. Marshall, S. J. Sara, and J. Born
Hippocampal Sharp Wave-Ripples Linked to Slow Oscillations in Rat Slow-Wave Sleep
J Neurophysiol,
July 1, 2006;
96(1):
62 - 70.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Jirsch, E. Urrestarazu, P. LeVan, A. Olivier, F. Dubeau, and J. Gotman
High-frequency oscillations during human focal seizures
Brain,
June 1, 2006;
129(6):
1593 - 1608.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. T. Barbe, H. Monyer, and R. Bruzzone
Cell-Cell Communication Beyond Connexins: The Pannexin Channels
Physiology,
April 1, 2006;
21(2):
103 - 114.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. D. Payne and L. Nadel
Sleep, dreams, and memory consolidation: The role of the stress hormone cortisol
Learn. Mem.,
November 1, 2004;
11(6):
671 - 678.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. P. Battaglia, G. R. Sutherland, and B. L. McNaughton
Hippocampal sharp wave bursts coincide with neocortical "up-state" transitions
Learn. Mem.,
November 1, 2004;
11(6):
697 - 704.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. O. Cunningham, D. M. Halliday, C. H. Davies, R. D. Traub, t. l. E. H. Buhl, and M. A. Whittington
Coexistence of gamma and high-frequency oscillations in rat medial entorhinal cortex in vitro
J. Physiol.,
September 1, 2004;
559(2):
347 - 353.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. A. Pennartz, E. Lee, J. Verheul, P. Lipa, C. A. Barnes, and B. L. McNaughton
The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples
J. Neurosci.,
July 21, 2004;
24(29):
6446 - 6456.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. A. Worrell, L. Parish, S. D. Cranstoun, R. Jonas, G. Baltuch, and B. Litt
High-frequency oscillations and seizure generation in neocortical epilepsy
Brain,
July 1, 2004;
127(7):
1496 - 1506.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. M. de la Prida and B. Gal
Synaptic Contributions to Focal and Widespread Spatiotemporal Dynamics in the Isolated Rat Subiculum In Vitro
J. Neurosci.,
June 16, 2004;
24(24):
5525 - 5536.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. G. Pelletier, J. Apergis, and D. Pare
Low-Probability Transmission of Neocortical and Entorhinal Impulses Through the Perirhinal Cortex
J Neurophysiol,
May 1, 2004;
91(5):
2079 - 2089.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Maier, V. Nimmrich, and A. Draguhn
Cellular and Network Mechanisms Underlying Spontaneous Sharp Wave-Ripple Complexes in Mouse Hippocampal Slices
J. Physiol.,
August 1, 2003;
550(3):
873 - 887.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. T. Dickson, G. Biella, and M. de Curtis
Slow Periodic Events and Their Transition to Gamma Oscillations in the Entorhinal Cortex of the Isolated Guinea Pig Brain
J Neurophysiol,
July 1, 2003;
90(1):
39 - 46.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Degenetais, A.-M. Thierry, J. Glowinski, and Y. Gioanni
Synaptic Influence of Hippocampus on Pyramidal Cells of the Rat Prefrontal Cortex: An In Vivo Intracellular Recording Study
Cereb Cortex,
July 1, 2003;
13(7):
782 - 792.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L M. De La Prida
Control of bursting by local inhibition in the rat subiculum in vitro
J. Physiol.,
May 15, 2003;
549(1):
219 - 230.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. M. Werk and C. A. Chapman
Long-term Potentiation of Polysynaptic Responses in Layer V of the Sensorimotor Cortex Induced by Theta-patterned Tetanization in the Awake Rat
Cereb Cortex,
May 1, 2003;
13(5):
500 - 507.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Sirota, J. Csicsvari, D. Buhl, and G. Buzsaki
Communication between neocortex and hippocampus during sleep in rodents
PNAS,
February 18, 2003;
100(4):
2065 - 2069.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. J. Staba, C. L. Wilson, A. Bragin, I. Fried, and J. Engel Jr
Quantitative Analysis of High-Frequency Oscillations (80-500 Hz) Recorded in Human Epileptic Hippocampus and Entorhinal Cortex
J Neurophysiol,
October 1, 2002;
88(4):
1743 - 1752.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Gais, M. Molle, K. Helms, and J. Born
Learning-Dependent Increases in Sleep Spindle Density
J. Neurosci.,
August 1, 2002;
22(15):
6830 - 6834.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. E N LeBeau, S. K Towers, R. D Traub, M. A Whittington, and E. H Buhl
Fast network oscillations induced by potassium transients in the rat hippocampus in vitro
J. Physiol.,
July 1, 2002;
542(1):
167 - 179.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Bragin, I. Mody, C. L. Wilson, and J. Engel Jr
Local Generation of Fast Ripples in Epileptic Brain
J. Neurosci.,
March 1, 2002;
22(5):
2012 - 2021.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Grenier, I. Timofeev, and M. Steriade
Focal Synchronization of Ripples (80-200 Hz) in Neocortex and Their Neuronal Correlates
J Neurophysiol,
October 1, 2001;
86(4):
1884 - 1898.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. P. Staff, H.-Y. Jung, T. Thiagarajan, M. Yao, and N. Spruston
Resting and Active Properties of Pyramidal Neurons in Subiculum and CA1 of Rat Hippocampus
J Neurophysiol,
November 1, 2000;
84(5):
2398 - 2408.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Venance, A. Rozov, M. Blatow, N. Burnashev, D. Feldmeyer, and H. Monyer
Connexin expression in electrically coupled postnatal rat brain neurons
PNAS,
August 10, 2000;
(2000)
160037097.
[Abstract]
[Full Text]
|
 |
|

|
 |

|
 |
 
R. D. Traub and A. Bibbig
A Model of High-Frequency Ripples in the Hippocampus Based on Synaptic Coupling Plus Axon-Axon Gap Junctions between Pyramidal Neurons
J. Neurosci.,
March 15, 2000;
20(6):
2086 - 2093.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Z. Nadasdy, H. Hirase, A. Czurko, J. Csicsvari, and G. Buzsaki
Replay and Time Compression of Recurring Spike Sequences in the Hippocampus
J. Neurosci.,
November 1, 1999;
19(21):
9497 - 9507.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. L. Morgan and T. J. Teyler
VDCCs and NMDARs Underlie Two Forms of LTP in CA1 Hippocampus In Vivo
J Neurophysiol,
August 1, 1999;
82(2):
736 - 740.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Csicsvari, H. Hirase, A. Czurko, A. Mamiya, and G. Buzsaki
Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat
J. Neurosci.,
January 1, 1999;
19(1):
274 - 287.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Funahashi and M. Stewart
Properties of {gamma}-frequency oscillations initiated by propagating population bursts in retrohippocampal regions of rat brain slices
J. Physiol.,
July 1, 1998;
510(1):
191 - 208.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. R. Bramham
Phasic Boosting of Medial Perforant Path-Evoked Granule Cell Output Time-Locked to Spontaneous Dentate EEG Spikes in Awake Rats
J Neurophysiol,
June 1, 1998;
79(6):
2825 - 2832.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kamondi, L. Acsady, and G. Buzsaki
Dendritic Spikes Are Enhanced by Cooperative Network Activity in the Intact Hippocampus
J. Neurosci.,
May 15, 1998;
18(10):
3919 - 3928.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Acsady, A. Kamondi, A. Sik, T. Freund, and G. Buzsaki
GABAergic Cells Are the Major Postsynaptic Targets of Mossy Fibers in the Rat Hippocampus
J. Neurosci.,
May 1, 1998;
18(9):
3386 - 3403.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. J. Chrobak and G. Buzsaki
Gamma Oscillations in the Entorhinal Cortex of the Freely Behaving Rat
J. Neurosci.,
January 1, 1998;
18(1):
388 - 398.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Kandel and G. Buzsaki
Cellular-Synaptic Generation of Sleep Spindles, Spike-and-Wave Discharges, and Evoked Thalamocortical Responses in the Neocortex of the Rat
J. Neurosci.,
September 1, 1997;
17(17):
6783 - 6797.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ceranik, R. Bender, J. R. P. Geiger, H. Monyer, P. Jonas, M. Frotscher, and J. Lubke
A Novel Type of GABAergic Interneuron Connecting the Input and the Output Regions of the Hippocampus
J. Neurosci.,
July 15, 1997;
17(14):
5380 - 5394.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D B Katz and J E Steinmetz
Single-unit evidence for eye-blink conditioning in cerebellar cortex is altered, but not eliminated, by interpositus nucleus lesions.
Learn. Mem.,
January 1, 1997;
4(1):
88 - 104.
[Abstract]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Venance, A. Rozov, M. Blatow, N. Burnashev, D. Feldmeyer, and H. Monyer
Connexin expression in electrically coupled postnatal rat brain neurons
PNAS,
August 29, 2000;
97(18):
10260 - 10265.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Csicsvari, H. Hirase, A. Czurko, A. Mamiya, and G. Buzsaki
Fast Network Oscillations in the Hippocampal CA1 Region of the Behaving Rat
J. Neurosci.,
August 15, 1999;
19(16):
RC20 - RC20.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Hirase, X. Leinekugel, J. Csicsvari, A. Czurko, and G. Buzsaki
Behavior-Dependent States of the Hippocampal Network Affect Functional Clustering of Neurons
J. Neurosci.,
May 15, 2001;
21(10):
RC145 - RC145.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|

|