Developmental regulation of active and passive membrane properties in rat vibrissa motoneurones

Abstract

We characterized the electrophysiological properties of vibrissa motoneurones (vMNs) in rat. Intracellular recordings of vMNs in brainstem slices from animals aged P4 to P5 and P9 to P11, i.e. newborn animals, showed that the subthreshold membrane impedance has the form of passive decay. In particular, the impedance follows the 1/ √ f signature for long dendrites beyond a cut-off frequency of f c = 8 Hz. In contrast, the impedance has the form of a resonant filter in vMNs from slices prepared from animals aged P17 to P23, i.e. young animals. The resonancehasapeaknear4Hzandanamplitudeof1.2timesthatatlowfrequencies(f ∼0.1 Hz). The low frequency onset of the resonance is shown to depend on a hyperpolarization-activated depolarizing current, I h . This current functions as a high-pass filter. The high frequency cut-off of the resonance results from passive decay in long dendrites, similar to the case with newborn animals but with f c = 20 Hz. In addition to a resonance in subthreshold properties, an enhanced resonance in spiking is observed in young as opposed to newborn animals. The transition from solely passive decay in vMNs from newborn animals to resonance in young animals coincides with the onset of whisking. Further, the width of the resonance encompasses the 4-15 Hz range of exploratory whisking. Nonetheless, it remains to be shown if there is a causal relation between the regulation of currents in vMNs and the onset of whisking. In particular, we further observed that the membrane impedance of hypoglossal motoneurones from both newborn and young animals exhibits a subthreshold resonance that also peaks near 4 Hz. The amplitude of this resonance increases from 1.1 to 1.4 times that at low frequencies in newborn versus young animals. We conjecture that resonance properties in vibrissa, hypoglossal, and potentially other motoneurones, may serve to transiently and purposely synchronize different orofacial behaviours.

Cellular mechanisms of motor control in the vibrissal system

“…The basic anatomy [25,26] and physiology [12,13,26] of the whisker musculature have been worked out, although detailed quantitative information is missing. Neurons in the lateral facial nucleus are the whisker motor neurons and some of their cellular properties might contribute to the rhythmicity of whisking [33,34]. Numerous structures provide input to the lateral facial nucleus, including the mysterious putative CPG.…”

“…As shown in Fig. 3a, their resonance properties [33] and the cellular effects of serotonergic inputs (Fig. 3b-e) [34] may predispose facial nucleus motor neurons to rhythmic discharges.…”

“…2a), the intrinsic whisker muscles (also referred to as vibrissal capsular muscle), has their points of attachment completely within The high impedance around whisking frequencies will predispose whisker facial nucleus motor neurons to respond to such frequencies. Modified from [33]. b-e Whole-cell current clamp recordings from a wFMN in response to intracellular injections of current pulses ranging from 110 to 60 pA, in 10-pA increments (b).…”

Resonant or Not, Two Amplification Modes of Proprioceptive Inputs by Persistent Inward Currents in Spinal Motoneurons

“…Resonance and I h current We report for the first time a subthreshold resonance in mammalian spinal motoneurons and provide evidence that I h underlies this resonance, as in many types of neurons (Hutcheon et al, 1996;Nguyen et al, 2004;Wu et al, 2005). (1) One hour after the application of a selective I h blocker (ZD-7288), we found no motoneuron displaying a subthreshold resonance.…”

Mixed Mode Oscillations in Mouse Spinal Motoneurons Arise from a Low Excitability State

“…MMOs have previously been reported in interneurons (Llinás et al, 1991) and pyramidal cells of the frontal cortex (Gutfreund et al, 1995), stellate cells of the entorhinal cortex Klink and Alonso, 1993), magnocellular neurons of the supraoptic nucleus (Boehmer et al, 2000), trigeminal mesencephalic neurons (Wu et al, 2001), striatal fast spiking interneurons (Bracci et al, 2003), and vibrissa motoneurons (Nguyen et al, 2004;Harish and Golomb, 2010). In some cases, they were shown to be associated with a subthreshold resonance due to a slowly activating potassium current and enhanced by the persistent sodium current (Gutfreund et al, 1995;Wu et al, 2001Wu et al, , 2005.…”