Intrinsic Theta-Frequency Membrane Potential Oscillations in Hippocampal CA1 Interneurons of Stratum Lacunosum-Moleculare

1999 ◽  
Vol 81 (3) ◽  
pp. 1296-1307 ◽  
Author(s):  
C. Andrew Chapman ◽  
Jean-Claude Lacaille
Keyword(s):  
Membrane Potential ◽  
Hippocampal Slices ◽  
Stratum Radiatum ◽  
Potential Oscillations ◽  
Spike Threshold ◽  
Hippocampal Ca1 ◽  
Theta Frequency ◽  
Stratum Lacunosum Moleculare ◽  
Membrane Potential Oscillations

Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare. The ionic conductances underlying membrane potential oscillations of hippocampal CA1 interneurons located near the border between stratum lacunosum-moleculare and stratum radiatum (LM) were investigated using whole cell current-clamp recordings in rat hippocampal slices. At 22°C, when LM cells were depolarized near spike threshold by current injection, 91% of cells displayed 2–5 Hz oscillations in membrane potential, which caused rhythmic firing. At 32°C, mean oscillation frequency increased to 7.1 Hz. Oscillations were voltage dependent and were eliminated by hyperpolarizing cells 6–10 mV below spike threshold. Blockade of ionotropic glutamate and GABA synaptic transmission did not affect oscillations, indicating that they were not synaptically driven. Oscillations were eliminated by tetrodotoxin, suggesting that Na+ currents generate the depolarizing phase of oscillations. Oscillations were not affected by blocking Ca2+ currents with Cd2+ or Ca2+-free ACSF or by blocking the hyperpolarization-activated current ( I h) with Cs+. Both Ba2+ and a low concentration of 4-aminopyridine (4-AP) reduced oscillations but TEA did not. Theta-frequency oscillations were much less common in interneurons located in stratum oriens. Intrinsic membrane potential oscillations in LM cells of the CA1 region thus involve an interplay between inward Na+ currents and outward K+ currents sensitive to Ba2+ and 4-AP. These oscillations may participate in rhythmic inhibition and synchronization of pyramidal neurons during theta activity in vivo.

Local Generation of Theta-Frequency EEG Activity in the Parasubiculum

2007 ◽  
Vol 97 (6) ◽  
pp. 3868-3879 ◽  
Author(s):  
Stephen D. Glasgow ◽  
C. Andrew Chapman
Keyword(s):  
Membrane Potential ◽  
Hippocampal Formation ◽  
Brain Slices ◽  
Stratum Radiatum ◽  
Potential Oscillations ◽  
Eeg Activity ◽  
Ca1 Region ◽  
Adjacent Structures ◽  
Theta Frequency ◽  
Membrane Potential Oscillations

The parasubiculum is a major component of the hippocampal formation that receives inputs from the CA1 region, anterior thalamus, and medial septum and that projects primarily to layer II of the entorhinal cortex. Hippocampal theta-frequency (4–12 Hz) electroencephalographic (EEG) activity has been correlated with sensorimotor integration, spatial navigation, and memory functions. The present study was aimed at determining if theta is also generated locally within the parasubiculum versus volume conducted from adjacent structures. In urethan-anesthetized rats, the phase-reversal of theta activity between superficial and deep layers of the parasubiculum was demonstrated using differential recordings from movable bipolar electrodes that eliminate the influence of volume-conducted activity. Parasubicular theta was abolished by atropine, and was in phase with theta in stratum radiatum/lacunosum-moleculare of the CA1 region. Whole cell current-clamp recordings in brain slices were then used to determine if parasubicular theta may be generated in part by membrane potential oscillations in layer II neurons. Membrane potential oscillations occurred in most layer II neurons, including four putative interneurons, when cells were held at near-threshold voltages using current injection. The frequency of oscillations increased from 3.2 to 6.1 Hz when bath temperature was raised from 22 to 32°C, and oscillations persisted in the presence of blockers of fast ionotropic glutamatergic and GABAergic synaptic transmission. Oscillations are therefore likely generated by intrinsic, voltage-dependent ionic conductances. These results indicate that theta field activity is generated locally within the parasubiculum and that intrinsic membrane potential oscillations, synchronized by local inhibitory inputs, may contribute to the generation of this activity.

scholarly journals Conductances Mediating Intrinsic Theta-Frequency Membrane Potential Oscillations in Layer II Parasubicular Neurons

2008 ◽  
Vol 100 (5) ◽  
pp. 2746-2756 ◽  
Author(s):  
Stephen D. Glasgow ◽  
C. Andrew Chapman
Keyword(s):  
Membrane Potential ◽  
Network Activity ◽  
Potential Oscillations ◽  
Cationic Current ◽  
Artificial Cerebrospinal Fluid ◽  
Theta Frequency ◽  
Ionic Conductances ◽  
Voltage Dependent ◽  
Cell Current ◽  
Membrane Potential Oscillations

Ionic conductances that generate membrane potential oscillations in neurons of layer II of the parasubiculum were studied using whole cell current-clamp recordings in horizontal slices from the rat brain. Blockade of ionotropic glutamate and GABA synaptic transmission did not reduce the power of the oscillations, indicating that oscillations are not dependent on synaptic inputs. Oscillations were eliminated when cells were hyperpolarized 6–10 mV below spike threshold, indicating that they are mediated by voltage-dependent conductances. Application of TTX completely eliminated oscillations, suggesting that Na+ currents are required for the generation of the oscillations. Oscillations were not reduced by blocking Ca2+ currents with Cd2+ or Ca2+-free artificial cerebrospinal fluid, or by blocking K+ conductances with either 50 μM or 5 mM 4-aminopyridine (4-AP), 30 mM tetraethylammonium (TEA), or Ba2+(1–2 mM). Oscillations also persisted during blockade of the muscarinic-dependent K+ current, IM, using the selective antagonist XE-991 (10 μM). However, oscillations were significantly attenuated by blocking the hyperpolarization-activated cationic current Ih with Cs+ and were almost completely blocked by the more potent Ih blocker ZD7288 (100 μM). Intrinsic membrane potential oscillations in neurons of layer II of the parasubiculum are therefore likely driven by an interaction between an inward persistent Na+ current and time-dependent deactivation of Ih. These voltage-dependent conductances provide a mechanism for the generation of membrane potential oscillations that can help support rhythmic network activity within the parasubiculum during theta-related behaviors.

Modelling the interrelations between calcium oscillations and ER membrane potential oscillations

1997 ◽  
Vol 63 (2-3) ◽  
pp. 221-239 ◽  
Author(s):  
Marko Marhl ◽  
Stefan Schuster ◽  
Milan Brumen ◽  
Reinhart Heinrich
Keyword(s):  
Membrane Potential ◽  
Calcium Oscillations ◽  
Potential Oscillations ◽  
Membrane Potential Oscillations ◽  
Er Membrane

Physiology and Morphology of Shared and Specialized Spinal Interneurons for Locomotion and Scratching

2008 ◽  
Vol 99 (6) ◽  
pp. 2887-2901 ◽  
Author(s):  
Ari Berkowitz
Keyword(s):  
Direct Evidence ◽  
Ventral Horn ◽  
Morphological Properties ◽  
Rhythmic Movements ◽  
Potential Oscillations ◽  
Spinal Interneurons ◽  
Firing Rates ◽  
Motor Outputs ◽  
Membrane Potential Oscillations

Distinct types of rhythmic movements that use the same muscles are typically generated largely by shared multifunctional neurons in invertebrates, but less is known for vertebrates. Evidence suggests that locomotion and scratching are produced partly by shared spinal cord interneuronal circuity, although direct evidence with intracellular recording has been lacking. Here, spinal interneurons were recorded intracellularly during fictive swimming and fictive scratching in vivo and filled with Neurobiotin. Some interneurons that were rhythmically activated during both swimming and scratching had axon terminal arborizations in the ventral horn of the hindlimb enlargement, indicating their likely contribution to hindlimb motor outputs during both behaviors. We previously described a morphological group of spinal interneurons (“transverse interneurons” or T neurons) that were rhythmically activated during all forms of fictive scratching at higher peak firing rates and with larger membrane potential oscillations than scratch-activated spinal interneurons with different dendritic orientations. The current study demonstrates that T neurons are activated during both swimming and scratching and thus are components of the shared circuitry. Many spinal interneurons activated during fictive scratching are also activated during fictive swimming (scratch/swim neurons), but others are suppressed during swimming (scratch-specialized neurons). The current study demonstrates that some scratch-specialized neurons receive strong and long-lasting hyperpolarizing inhibition during fictive swimming and are also morphologically distinct from T neurons. Thus this study indicates that locomotion and scratching are produced by a combination of shared and dedicated interneurons whose physiological and morphological properties are beginning to be revealed.

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