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

Abstract

Glasgow SD, Chapman CA. Conductances mediating intrinsic thetafrequency membrane potential oscillations in layer II parasubicular neurons. J Neurophysiol 100: 2746 -2756, 2008. First published September 24, 2008 doi:10.1152/jn.90351.2008. 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 ϩ currents are required for the generation of the oscillations. Oscillations were not reduced by blocking Ca 2ϩ currents with Cd 2ϩ or Ca 2ϩ -free artificial cerebrospinal fluid, or by blocking K ϩ conductances with either 50 M or 5 mM 4-aminopyridine (4-AP), 30 mM tetraethylammonium (TEA), or Ba 2ϩ (1-2 mM). Oscillations also persisted during blockade of the muscarinic-dependent K ϩ current, I M , using the selective antagonist XE-991 (10 M). However, oscillations were significantly attenuated by blocking the hyperpolarization-activated cationic current I h with Cs ϩ and were almost completely blocked by the more potent I h blocker ZD7288 (100 M). Intrinsic membrane potential oscillations in neurons of layer II of the parasubiculum are therefore likely driven by an interaction between an inward persistent Na ϩ current and time-dependent deactivation of I h . 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.

Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy

“…Future experiments may test the causal role of OFC theta oscillatory activity in the acquisition and reversal of learned associations, for instance by local infusions of substances that were shown to alter oscillations in other brain structures [e.g., GABA B and muscarinic receptor antagonists (Leung and Shen, 2007) as well as blockers of I h (Glasgow and Chapman, 2008)]. Second, further experiments may examine whether information on negative outcome predictions is also temporally structured by way of oscillatory activity, and how positive predictions about noningestible rewards are coded.…”

Contribution of Ih to the relative facilitation of synaptic responses induced by carbachol in the entorhinal cortex during repetitive stimulation of the parasubiculum

“…Acetylcholine plays a role in the generation of theta and gamma rhythm EEG activities in both the entorhinal cortex and parasubiculum (Mitchell and Ranck, 1980;Dickson et al 2000a;Glasgow and Chapman, 2007;Tsuno et al, 2013) in part by depolarizing neurons to near-threshold voltage levels (Klink and Alonso 1997;Dickson et al 2000b;Hasselmo 2006;Glasgow and Chapman, 2008). Theta and gamma activities co-occur and are thought to contribute to mechanisms of spatial navigation and learning and memory in the hippocampal formation, entorhinal cortex and parasubiculum (Buzsaki, 2002;Hasselmo, 2006;Igarashi et al, 2014;Yamamoto et al, 2014) and the coordination of firing among place and grid cells (O'Keefe and Recce, 1993;Taube, 1995;Hasselmo et al, 2007;Boccara et al, 2010).…”

Disentanglement of local field potential sources by independent component analysis

“…A more defying problem is the contribution of intrinsic currents to LFPs (e.g., Murakami et al 2003;Glasgow and Chapman 2008). If such contribution were strong enough to initiate active propagation of currents within dendrites, the assumption of stationary currents required for ICA application would be challenged and we would have to admit a certain error in the curves of spatial weights obtained for isolated LFP generators.…”