Synaptic Activation of Plateaus in Hindlimb Motoneurons of Decerebrate Cats

Abstract

Intracellular recordings were made from hindlimb motoneurons in decerebrate cats to study how synaptic inputs could affect the threshold at which plateau potentials are activated with current injections through the recording microelectrode in the cell body. This study was prompted by recent evidence that the noninactivating inward currents that regeneratively produce the plateau potentials arise (partly) from dendritic conductances, which may be relatively more accessible to synaptic input than to current injected into the soma. Initially, cells were studied by injecting a slow triangular current ramp intracellularly to determine the threshold for activation of the plateau. In cells where the sodium spikes were blocked with intracellular QX314, plateau activation was readily seen as a sudden jump in membrane potential, which was not directly reversed as the current was decreased. With normal spiking, the plateau activation (the noninactivating inward current) was reflected by a steep and sustained jump in firing rate that was not directly reversed as the current was decreased. Importantly, the threshold for plateau activation (at 34 Hz on average) was significantly above the recruitment level (13 Hz on average). When tonic synaptic excitation [excitatory postsynaptic potentials (EPSPs)] was provided either by stretching the triceps surae muscle or by stimulating its nerve at a high frequency, the threshold for plateau activation by intracellular current injection was significantly lowered (by 12 Hz or 5.8 mV on average, without and with QX314, respectively). Conversely, tonic synaptic inhibition [inhibitory postsynaptic potentials (IPSPs)], provided by appropriate nerve stimulation, significantly raised the plateau threshold (by 19 Hz or 7.6 mV on average). These effects were graded with the intensity of tonic EPSPs and IPSPs. Strong enough EPSPs brought the plateau threshold down sufficiently that it was activated by the intracellular current soon after recruitment. A further increase in tonic EPSPs recruited the cell directly, and in this case the plateau was activated at or before recruitment. The finding that synaptic excitation can produce plateau activation below the recruitment level is of importance for the interpretation of its function. With this low-threshold activation, the plateau potentials are likely important in securing an effective recruitment to frequencies that produce significant force generation and would subsequently have no further affect on the frequency modulation, other than to provide a steady depolarizing bias that would help to sustain firing (cf. self-sustained firing). Additional jumps in frequency after recruitment (i.e., bistable firing) would not be expected.

Beginning at the end: Repetitive firing properties in the final common pathway

“…Heckman and Robert Lee demonstrated that the synaptic current evoked by group Ia afferent stimulation was enhanced by methoxamine application (which can lead to plateau potentials; Lee & Heckman, 1996), David Bennett together with Hultborn and colleagues demonstrated that the threshold current for activating plateau potentials was much lower when the motoneurons were synaptically activated by Ia afferent stimulation. This finding was consistent with activation of these currents near the site of the synaptic input, i.e., on the dendrites (Bennett et al, 1998). Using somatic voltage clamp of mouse motoneurons in spinal cord slice preparations (Carlin et al, 2000a), we demonstrated delayed inward currents in response to step depolarizations and suggested that the delay was caused by the dendritic location of the conductances (Carlin et al, 2000b; see also Booth and Rinzel, 1995;Booth et al, 1997;Muller and Lux, 1993).…”

Differential contributions of somatic and dendritic calcium-dependent potassium currents to the control of motoneuron excitability following spinal cord injury

“…PIC activation may be facilitated by increased excitatory reflexes following spinal cord injury (Baker and Chandler 1987;Li et al 2004b). Synaptic inhibition has been shown to be a key mechanism in the control of motoneuron discharge and dendritic PIC activation (Bennett et al 1998;Hultborn et al 2003), particularly for dendritic sources of inhibition (Bui et al 2008;Venugopal et al 2011). Synaptic inhibition may be altered by changes in inhibitory receptors (Bareyre and Schwab 2003;Khristy et al 2009) and alterations in the strength of segmental inhibitory synaptic inputs (Shapiro 1997;Norton et al 2008).…”

Staircase Currents in Motoneurons: Insight into the Spatial Arrangement of Calcium Channels in the Dendritic Tree

“…The activation of dendritic persistent inward currents in motoneurons can lead to the production of electrical events known as plateau potentials (Schwindt and Crill, 1980;Hounsgaard and Kiehn, 1993;Lee and Heckman, 1996;Bennett et al, 1998). We first investigated whether calcium-dependent plateau potentials could be produced by mouse motoneurons.…”

“…However, voltage-activated calcium currents in motoneuron dendrites, which generate "persistent inward currents" (PICs), appear to ensure integration of even distal inputs Li and Bennett, 2003). PICs generate plateau potentials (Hounsgaard and Kiehn, 1989;Lee and Heckman, 1996) and amplify synaptic inputs to motoneurons, both excitatory (Brownstone et al, 1994;Bennett et al, 1998;Lee and Heckman, 2000;Jones and Lee, 2006;Powers et al, 2008) and inhibitory (Hultborn et al, 2003;Kuo et al, 2003;Bui et al, 2008a).…”