 |
||||
|
||||
|
||||
|
||||
|
||||
The Journal of Neuroscience, October 13, 2004, 24(41):9127-9137; doi:10.1523/JNEUROSCI.2113-04.2004
Previous Article | Next Article
Behavioral/Systems/Cognitive
Spike Timing of Distinct Types of GABAergic Interneuron during Hippocampal Gamma Oscillations In Vitro
Norbert Hájos,1 János Pálhalmi,1 Edward O. Mann,2 Beáta Németh,1 Ole Paulsen,2 andTamas F. Freund1 1Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest H-1450, Hungary, and 2Department of Physiology, University of Oxford, Parks Road, Oxford OX1 3PT, United Kingdom
Gamma frequency (30-100 Hz) network oscillations occur in the intact hippocampus during awake, attentive behavior. Here, we explored the underlying cellular mechanisms in an in vitro model of persistent gamma-frequency oscillations, induced by bath application of 20 µM carbachol in submerged hippocampal slices at 30 ± 1°C. Current-source density analysis of the field oscillation revealed a prominent alternating sink-source pair in the perisomatic and apical dendritic regions of CA3. To elucidate the active events generating these extracellular dipoles, we examined the firing properties of distinct neuron types. Visually guided unit recordings were obtained from individual CA3 neurons followed by intracellular labeling for anatomical identification. Pyramidal cells fired at 2.82 ± 0.7 Hz, close to the negative peak of the oscillation (0.03 ± 0.65 msec), and often in conjunction with a negative spike-like component of the field potential. In contrast, all phase-coupled interneurons fired after this negative peak. Perisomatic inhibitory interneurons fired at high frequency (18.1 ± 2.7 Hz), shortly after the negative peak (1.97 ± 0.95 msec) and were strongly phase-coupled. Dendritic inhibitory interneurons fired at lower frequency (8.4 ± 2.4 Hz) and with less fidelity and a longer delay after the negative peak (4.3 ± 1.1 msec), whereas interneurons with cell body in the stratum radiatum often showed no phase relationship with the field oscillation. The phase and spike time data of individual neurons, together with the current-source density analysis, support a synaptic feedback model of gamma oscillations primarily involving pyramidal cells and inhibitory cells targeting their perisomatic region.
Key words: hippocampus; carbachol; gamma oscillation; GABAergic cells; phase-coupling; rat
Received June 1, 2004; revised August 12, 2004; accepted August 31, 2004.
This article has been cited by other articles:
P. Wulff, A. A. Ponomarenko, M. Bartos, T. M. Korotkova, E. C. Fuchs, F. Bahner, M. Both, A. B. L. Tort, N. J. Kopell, W. Wisden, et al.
Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons
PNAS, March 3, 2009; 106(9): 3561 - 3566.
[Abstract] [Full Text] [PDF]
S. Middleton, J. Jalics, T. Kispersky, F. E. N. LeBeau, A. K. Roopun, N. J. Kopell, M. A. Whittington, and M. O. Cunningham
NMDA receptor-dependent switching between different gamma rhythm-generating microcircuits in entorhinal cortex
PNAS, November 25, 2008; 105(47): 18572 - 18577.
[Abstract] [Full Text] [PDF]
N. V. Povysheva, A. V. Zaitsev, D. C. Rotaru, G. Gonzalez-Burgos, D. A. Lewis, and L. S. Krimer
Parvalbumin-Positive Basket Interneurons in Monkey and Rat Prefrontal Cortex
J Neurophysiol, October 1, 2008; 100(4): 2348 - 2360.
[Abstract] [Full Text] [PDF]
M. Galarreta, F. Erdelyi, G. Szabo, and S. Hestrin
Cannabinoid Sensitivity and Synaptic Properties of 2 GABAergic Networks in the Neocortex
Cereb Cortex, October 1, 2008; 18(10): 2296 - 2305.
[Abstract] [Full Text] [PDF]
A. K. Roopun, M. O. Cunningham, C. Racca, K. Alter, R. D. Traub, and M. A. Whittington
Region-Specific Changes in Gamma and Beta2 Rhythms in NMDA Receptor Dysfunction Models of Schizophrenia
Schizophr Bull, September 1, 2008; 34(5): 962 - 973.
[Abstract] [Full Text] [PDF]
G. Gonzalez-Burgos and D. A. Lewis
GABA Neurons and the Mechanisms of Network Oscillations: Implications for Understanding Cortical Dysfunction in Schizophrenia
Schizophr Bull, September 1, 2008; 34(5): 944 - 961.
[Abstract] [Full Text] [PDF]
T. Klausberger and P. Somogyi
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Science, July 4, 2008; 321(5885): 53 - 57.
[Abstract] [Full Text] [PDF]
F. Manseau, R. Goutagny, M. Danik, and S. Williams
The Hippocamposeptal Pathway Generates Rhythmic Firing of GABAergic Neurons in the Medial Septum and Diagonal Bands: An Investigation Using a Complete Septohippocampal Preparation In Vitro
J. Neurosci., April 9, 2008; 28(15): 4096 - 4107.
[Abstract] [Full Text] [PDF]
T. J. Senior, J. R. Huxter, K. Allen, J. O'Neill, and J. Csicsvari
Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus
J. Neurosci., February 27, 2008; 28(9): 2274 - 2286.
[Abstract] [Full Text] [PDF]
J. Epsztein, Y. Ben-Ari, A. Represa, and V. Crepel
Late-Onset Epileptogenesis and Seizure Genesis: Lessons From Models of Cerebral Ischemia
Neuroscientist, February 1, 2008; 14(1): 78 - 90.
[Abstract] [PDF]
C. Huchzermeyer, K. Albus, H.-J. Gabriel, J. Otahal, N. Taubenberger, U. Heinemann, R. Kovacs, and O. Kann
Gamma Oscillations and Spontaneous Network Activity in the Hippocampus Are Highly Sensitive to Decreases in pO2 and Concomitant Changes in Mitochondrial Redox State
J. Neurosci., January 30, 2008; 28(5): 1153 - 1162.
[Abstract] [Full Text] [PDF]
M. L. Lorincz, V. Crunelli, and S. W. Hughes
Cellular Dynamics of Cholinergically Induced {alpha} (8 13 Hz) Rhythms in Sensory Thalamic Nuclei In Vitro
J. Neurosci., January 16, 2008; 28(3): 660 - 671.
[Abstract] [Full Text] [PDF]
L. de Almeida, M. Idiart, and J. E. Lisman
Memory retrieval time and memory capacity of the CA3 network: Role of gamma frequency oscillations
Learn. Mem., November 15, 2007; 14(11): 795 - 806.
[Abstract] [Full Text] [PDF]
M. Goldin, J. Epsztein, I. Jorquera, A. Represa, Y. Ben-Ari, V. Crepel, and R. Cossart
Synaptic Kainate Receptors Tune Oriens-Lacunosum Moleculare Interneurons to Operate at Theta Frequency
J. Neurosci., September 5, 2007; 27(36): 9560 - 9572.
[Abstract] [Full Text] [PDF]
A. Baude, C. Bleasdale, Y. Dalezios, P. Somogyi, and T. Klausberger
Immunoreactivity for the GABAA Receptor {alpha}1 Subunit, Somatostatin and Connexin36 Distinguishes Axoaxonic, Basket, and Bistratified Interneurons of the Rat Hippocampus
Cereb Cortex, September 1, 2007; 17(9): 2094 - 2107.
[Abstract] [Full Text] [PDF]
J. J. Tukker, P. Fuentealba, K. Hartwich, P. Somogyi, and T. Klausberger
Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo
J. Neurosci., August 1, 2007; 27(31): 8184 - 8189.
[Abstract] [Full Text] [PDF]
J. Spampanato and I. Mody
Spike Timing of Lacunosom-Moleculare Targeting Interneurons and CA3 Pyramidal Cells During High-Frequency Network Oscillations In Vitro
J Neurophysiol, July 1, 2007; 98(1): 96 - 104.
[Abstract] [Full Text] [PDF]
A. Bibbig, S. Middleton, C. Racca, M. J. Gillies, H. Garner, F. E. N. LeBeau, C. H. Davies, and M. A. Whittington
Beta Rhythms (15-20 Hz) Generated by Nonreciprocal Communication in Hippocampus
J Neurophysiol, April 1, 2007; 97(4): 2812 - 2823.
[Abstract] [Full Text] [PDF]
T. Radman, Y. Su, J. H. An, L. C. Parra, and M. Bikson
Spike Timing Amplifies the Effect of Electric Fields on Neurons: Implications for Endogenous Field Effects
J. Neurosci., March 14, 2007; 27(11): 3030 - 3036.
[Abstract] [Full Text] [PDF]
I. Oren, E. O. Mann, O. Paulsen, and N. Hajos
Synaptic Currents in Anatomically Identified CA3 Neurons during Hippocampal Gamma Oscillations In Vitro
J. Neurosci., September 27, 2006; 26(39): 9923 - 9934.
[Abstract] [Full Text] [PDF]
J. Epsztein, M. Milh, R. Id Bihi, I. Jorquera, Y. Ben-Ari, A. Represa, and V. Crepel
Ongoing epileptiform activity in the post-ischemic hippocampus is associated with a permanent shift of the excitatory-inhibitory synaptic balance in CA3 pyramidal neurons.
J. Neurosci., June 28, 2006; 26(26): 7082 - 7092.
[Abstract] [Full Text] [PDF]
V. S. Sohal and J. R. Huguenard
Inhibitory coupling specifically generates emergent gamma oscillations in diverse cell types
PNAS, December 20, 2005; 102(51): 18638 - 18643.
[Abstract] [Full Text] [PDF]
M. C. Gravielle, R. Faris, S. J. Russek, and D. H. Farb
GABA Induces Activity Dependent Delayed-onset Uncoupling of GABA/Benzodiazepine Site Interactions in Neocortical Neurons
J. Biol. Chem., June 3, 2005; 280(22): 20954 - 20960.
[Abstract] [Full Text] [PDF]
E. O. Mann, C. A. Radcliffe, and O. Paulsen
Hippocampal gamma-frequency oscillations: from interneurones to pyramidal cells, and back
J. Physiol., January 1, 2005; 562(1): 55 - 63.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|