Slow Conductances Could Underlie Intrinsic Phase-Maintaining Properties of Isolated Lobster (Panulirus interruptus) Pyloric Neurons

Abstract

The rhythmic pyloric network of the lobster stomatogastric system approximately maintains phase (that is, the burst durations and durations between the bursts of its neurons change proportionally) when network cycle period is altered by current injection into the network pacemaker (Hooper, 1997a,b). When isolated from the network and driven by rhythmic hyperpolarizing current pulses, the delay to firing after each pulse of at least one network neuron type [pyloric (PY)] varies in a phase-maintaining manner when cycle period is varied (Hooper, 1998). These variations require PY neurons to have intrinsic mechanisms that respond to changes in neuron activity on time scales at least as long as 2 s. Slowly activating and deactivating conductances could provide such a mechanism. We tested this possibility by building models containing various slow conductances. This work showed that such conductances could indeed support intrinsic phase maintenance, and we show here results for one such conductance, a slow potassium conductance. These conductances supported phase maintenance because their mean activation level changed, hence altering neuron postinhibition firing delay, when the rhythmic input to the neuron changed. Switching the sign of the dependence of slow-conductance activation and deactivation on membrane potential resulted in neuron delays switching to change in an anti-phase-maintaining manner. These data suggest that slow conductances or similar slow processes such as changes in intracellular Ca 2ϩ concentration could underlie phase maintenance in pyloric network neurons.

Slow and Persistent Postinhibitory Rebound Acts as an Intrinsic Short-Term Memory Mechanism

“…4). Hooper et al (2009) found some of the same effects reported here, but did not examine changes in spike rate during long trains of inhibitory inputs, or look at the effects of changing DCI while holding period fixed. Thus our results are consistent with previous work, but reveal additional dimensions of the effects of rhythmic inhibition on excitability.…”

Animal-to-Animal Variability in Neuromodulation and Circuit Function

“…The mechanisms that underlie the maintenance of phase over this range of frequencies have intrigued investigators, because membrane and synaptic currents have characteristic time constants, which would tend to create fixed delays, not constant phase (Hooper 1998; Manor et al 2003; Hooper et al 2009; Tang et al 2010), and it is thought that phase maintenance requires the interaction of multiple synaptic and intrinsic conductances (Manor et al 2003; Tang et al 2010). …”

Sound Rhythms Are Encoded by Postinhibitory Rebound Spiking in the Superior Paraolivary Nucleus

“…The variability in the number of spikes observed during the rebound could be related to the relative amount of T-type Ca 2+ currents or the expression of Cav3 channel subtypes in SPON neurons, as has been reported in postinhibitory rebound firing in deep cerebellar nuclei (Molineux et al, 2006). The fact that RDs trigger very few spikes in the SPON implies that additional ion conductances, such as voltage-gated K + channels (Kanold and Manis, 2001; Hooper et al, 2009) or Ca 2+ -activated K + channels (Kim and Trussell, 2007) that activate at more depolarized voltages, may influence the timing and/or the duration of the rebound response. In addition, geometrical variations in the size or the number of dendrites (Mainen and Sejnowski, 1996) or synaptic activity levels could influence the shape of the rebound response.…”