Activity-dependent plasticity in desecending synaptic inputs to spinal motoneurons in an in vitro turtle brainstem-spinal cord preparation

Long-term (>1 h) and short-term (sec-to-min) activity-dependent synaptic plasticity have been proposed to contribute to the patterning of rhythmic network activity. There is, however, very little experimental evidence to support this hypothesis. Previously, we demonstrated that electrically-evoked descending synaptic inputs to respiratory-related spinal motoneurons express long-term depression (LTD) or long-term potentiation (LTP) following spinal stimulation at different frequencies in an in vitro turtle brainstem-spinal cord preparation [1]. For example, evoked potentials in pectoralis (expiratory) nerves express LTD following 1 and 10 Hz spinal stimulation (900 pulses), while potentials in serratus (inspiratory) nerves express LTP following 100 Hz spinal stimulation (900 pulses).

In this study, we hypothesized that activity-dependent synaptic plasticity is expressed in identified synaptic connections within the respiratory control system of adult turtles (Pseudemys), and that LTD is expressed in respiratory descending synaptic inputs to pectoralis motoneurons following 10 Hz spinal stimulation. Using in vitro turtle brainstem-spinal cord preparations (n = 6), the lateral funiculus at spinal segment C5 (rostral to pectoralis and serratus motoneurons) was electrically stimulated (10 Hz, 900 pulses, 400 μA) while the preparation spontaneously produced rhythmic respiratory motor output. One application of spinal stimulation immediately decreased respiratory burst amplitude by ~75% on both pectoralis and serratus (P < 0.05), but amplitudes returned to pre-stim levels within 30 min. Thus, 10 Hz spinal stimulation produces short-term depression of expiratory and inspiratory motor output. In separate experiments (n = 5), three episodes of 10 Hz conditioning stimulation (separated by 5 min) nearly abolished pectoralis and serratus burst amplitudes during stimulation (P < 0.05). Pectoralis bursts returned to pre-stimulus levels within 30 min, but serratus bursts returned to pre-stimulus levels within 20 min and tended to exceed pre-stim levels by 30–40% at 50 min after conditioning (P > 0.05). Closer examination showed that serratus burst amplitudes at 50 min post-stim were depressed by ~20% in 3/5 preparations, and potentiated by 100–150% in 2/5 preparations. Spinal stimulation did not change hypoglossal burst amplitude.

In conclusion, 10 Hz spinal stimulation did not exclusively elicit LTD in spontaneous expiratory activity in pectoralis nerves, suggesting that LTD is expressed in nonrespiratory-related descending synaptic inputs to pectoralis motoneurons, or that spontaneous respiratory activity in pectoralis motoneurons overrides the expression of LTD. We hypothesize that the activity-dependent plasticity observed with spinal stimulation is due to spinal mechanisms because hypoglossal respiratory activity was unaltered.