Influence of Active Dendritic Currents on Input-Output Processing in Spinal Motoneurons In Vivo

Abstract

The extensive dendritic tree of the adult spinal motoneuron generates a powerful persistent inward current (PIC). We investigated how this dendritic PIC influenced conversion of synaptic input to rhythmic firing. A linearly increasing, predominantly excitatory synaptic input was generated in triceps ankle extensor motoneurons by slow stretch (duration: 2-10 s) of the Achilles tendon in the decerebrate cat preparation. The firing pattern evoked by stretch was measured by injecting a steady current to depolarize the cell to threshold for firing. The effective synaptic current (I(N), the net synaptic current reaching the soma of the cell) evoked by stretch was measured during voltage clamp. Hyperpolarized holding potentials were used to minimize the activation of the dendritic PIC and thus estimate stretch-evoked I(N) for a passive dendritic tree (I(N,PASS)). Depolarized holding potentials that approximated the average membrane potential during rhythmic firing allowed strong activation of the dendritic PIC and thus resulted in marked enhancement of the total stretch-evoked I(N) (I(N,TOT)). The net effect of the dendritic PIC on the generation of rhythmic firing was assessed by plotting stretch-evoked firing (strong PIC activation) versus stretch-evoked I(N,PASS) (minimal PIC activation). The gain of this input-output function for the neuron (I-O(N)) was found to be ~2.7 times as high as for the standard injected frequency current (F-I) function in low-input conductance neurons. However, about halfway through the stretch, firing rate tended to become constant, resulting in a sharp saturation in I-O(N) that was not present in F-I. In addition, the gain of I-O(N) decreased sharply with increasing input conductance, resulting in much lower stretch-evoked firing rates in high-input conductance cells. All three of these phenomena (high initial gain, saturation, and differences in low- and high-input conductance cells) were also readily apparent in the differences between stretch-evoked I(N,TOT) and I(N, PASS) and thus could be accounted for by the activation of the dendritic PIC. As a result, stretch-evoked I(N,TOT) and F-I provided an accurate prediction of the overall change in stretch-evoked firing. However, in about half of the low-input conductance cells, the rate of rise of firing in response to stretch was not smoothly graded but instead consisted of a rapid surge. Stretch-evoked I(N,TOT) was always smoothly graded. This suggests that although stretch-evoked I(N,TOT) can be used to predict the overall change in firing, prediction of the dynamics of firing may be less accurate.

High-frequency submaximal stimulation over muscle evokes centrally generated forces in human upper limb skeletal muscles

“…Muscle stimulation at 20 Hz presumably elicits ionotropic synaptic currents that are influenced by plateau potentials (21) in spinal motoneurons and interneurones. The total synaptic current from stretch-related afferents is larger in smaller motoneurons, and, for the same level of stretch-activated input, the firing frequency is larger in small than large motoneurons (36). If a motoneuron plateau potential was present, the gain shift in the input-output characteristic of the motoneuron would increase firing frequency depending on motoneuron size, and the result could be indistinguishable from increased synaptic input.…”

“…Despite the simplicity of this method, it has limitations relevant to our paradigm that prevented us from using this technique. There can be saturation in firing frequency of human motor units (13), and there is smaller amplification (36) and larger current leakage in high-threshold motoneurons (compared with low-threshold ones) during plateau potentials (21). Muscle stimulation at 20 Hz presumably elicits ionotropic synaptic currents that are influenced by plateau potentials (21) in spinal motoneurons and interneurones.…”

Characteristics and Organization of Discharge Properties in Rat Hindlimb Motoneurons

“…L-type Ca 2ϩ PICs are also activated below or at threshold in many motoneurons in states of increased PIC expression (Lee and Heckman 1998b;Li et al 2004), helping to initiate and sustain discharge. Moreover, by amplifying synaptic inputs, PICs can significantly increase the gain of motoneurons (Lee et al 2003).…”

“…The intrinsic properties of motoneurons are subject to several sources of neuromodulation (Rekling et al 2000) and PIC expression is dependent on monoamines (Hounsgaard and Kiehn 1989;Hounsgaard et al 1988;Lee and Heckman 2000;). Changes in the intrinsic properties of motoneurons could contribute to abnormal manifestations of motor control.…”

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

“…Both persistent inward currents (PICs) may augment the effective synaptic current that reaches the spike initiation zone of motoneurons (Powers and Binder, 2001;Prather et al, 2001;Lee et al, 2003), thereby increasing the firing frequency (Lee and Heckman, 2000;Hultborn et al, 2003;Lee et al, 2003). In cat spinal motoneurons, they can amplify synaptic inputs elicited by muscle stretches or tendon vibration (Bennett et al, 1998;Lee and Heckman, 2000;Jones and Lee, 2006).…”