Spike Resonance Properties in Hippocampal O-LM Cells Are Dependent on Refractory Dynamics

Abstract

During a wide variety of behaviors, hippocampal field potentials show significant power in the theta (4–12 Hz) frequency range and individual neurons commonly phase-lock with the 4–12 Hz field potential. The underlying cellular and network mechanisms that generate the theta rhythm, however, are poorly understood. Oriens-lacunosum moleculare (O-LM) interneurons have been implicated as crucial contributors to generating theta in local hippocampal circuits because of their unique axonal projections, slow synaptic kinetics and the fact that spikes are phase locked to theta field potentials in vivo. We performed experiments in brain slice preparations from Long-Evans rats to investigate the ability of O-LM cells to generate phase-locked spike output in response to artificial synaptic inputs. We find that O-LM cells do not respond with any preference in spike output at theta frequencies when injected with broadband artificial synaptic inputs. However, when presented with frequency-modulated inputs, O-LM spike output shows the ability to phase-lock well to theta-modulated inputs, despite their strong low-pass profiles of subthreshold membrane impedance. This result was dependent on spike refractory dynamics and could be controlled by real-time manipulation of the post-spike afterhyperpolarization. Finally, we show that the ability of O-LM cells to phase-lock well to theta-rich inputs is independent of the h-current, a membrane mechanism often implicated in the generation of theta frequency activity.

Frequency-invariant temporal ordering of interneuronal discharges during hippocampal oscillations in awake mice

“…PVBCs fire fast, nonaccommodating action potentials and have fast membrane time constants, and GABA-release from their axon terminals takes place in a synchronous manner with tight temporal association between the presynaptic action potential and the postsynaptic response (38,39). OLM cells receive their primary, markedly facilitating excitatory inputs from local CA1 pyramidal cells with minimal input from CA3 pyramidal cell axon collaterals (40,41), and their intrinsic biophysical properties are thought to enable them to participate preferentially in theta-frequency activity (42)(43)(44)(45)(46). Therefore, by focusing on PVBCs and OLM cells, the present study aimed to determine the temporal structure of spiking activity of two key sources of perisomatic and distal dendritic GABAergic input to CA1 pyramidal cells under anesthesia-free conditions and across a range of network oscillatory frequencies spanning a wide range from <10 Hz to >100 Hz, with four specific frequency bands associated with distinct behavioral states and functions.…”

Frequency preference in two-dimensional neural models: a linear analysis of the interaction between resonant and amplifying currents

“…A large number of studies in recent years has focused on subthreshold membrane resonance in neurons, its dependence on ionic currents and its influence on neuronal and network oscillations (Richardson et al 2003; Ledoux and N. 2011; Castro-Alamancos et al 2007; Tohidi and Nadim 2009; Izhikevich et al 2003; Engel et al 2008; Reinker et al 2004; Kispersky et al 2012; Moca et al 2012; Thevenin et al 2011). Subthreshold membrane resonance is primarily described on the basis of a linear RLC circuit where R is equated with the membrane resistance, C with the membrane capacitance and the inductance L , more abstractly, with voltage-gated ionic conductance properties (Erchova et al 2004).…”

Parvalbumin Interneurons of Hippocampus Tune Population Activity at Theta Frequency

“…SOM Interneurons Modulate TA Inputs SOM interneurons have long been foreseen as instrumental in hippocampal theta generation (Gloveli et al, 2005) (but see Kispersky et al, 2012). In addition, recent work has demonstrated that SOM interneurons influence the probability of PC burst firing (Lovett-Barron et al, 2012;Royer et al, 2012).…”