Recovery of inspiratory intercostal muscle activity following high cervical hemisection

Abstract

Anatomical and neurophysiological evidence indicates that thoracic interneurons can serve a commissural function and activate contralateral motoneurons. Accordingly, we hypothesized that respiratory-related intercostal (IC) muscle electromyogram (EMG) activity would be only modestly impaired by a unilateral cervical spinal cord injury. Inspiratory tidal volume (VT) was recorded using pneumotachography and EMG activity was recorded bilaterally from the 1st to 2nd intercostal space in anesthetized, spontaneously breathing rats. Studies were conducted at 1-3 days, 2 wks or 8 wks following C2 spinal cord hemisection (C2HS). Data were collected during baseline breathing and a brief respiratory challenge (7% CO(2)). A substantial reduction in inspiratory intercostal EMG bursting ipsilateral to the lesion was observed at 1-3 days post-C2HS. However, a time-dependent return of activity occurred such that by 2 wks post-injury inspiratory intercostal EMG bursts ipsilateral to the lesion were similar to age-matched, uninjured controls. The increases in ipsilateral intercostal EMG activity occurred in parallel with increases in VT following the injury (R=0.55; P<0.001). We conclude that plasticity occurring within a "crossed-intercostal" circuitry enables a robust, spontaneous recovery of ipsilateral intercostal activity following C2HS in rats.

Fig. 1

The effects of C2HS on ventilation. Acutely following C2HS (i.e. 1–3 days) rats exhibited reduced frequency (fR), tidal volume (VT) and minute ventilation (VE) during baseline and hypercapnic challenge. Two weeks post-C2HS, a transient elevation in fR was noted during both conditions (A) triggering enhanced VE during baseline (D and E), while VT returned to control levels (B and C). Normalization of fR (A) and sustained VT recovery (B and C) persisted at 8 wks post-C2HS. VT and VE are expressed as mean values (B and D) and mean values relative to body mass (C and E). ***P < 0.001, **P < 0.01, *P < 0.05 from baseline values; ^###P < 0.001 from all other groups; ^†††P < 0.001, ^††P < 0.01, ^†P < 0.05 from 1–3 days C2HS group.

Fig. 2

Examples of rostral inspiratory intercostal EMG during poikilocapnic baseline and hypercapnic respiratory challenge. The images show the raw (EMG) and integrated EMG (∫ EMG) signals from a control (uninjured) rat, and rats studied 3 days, 2 wks and 8 wks following C2HS injury. C2HS resulted in decreased ipsilateral EMG activity 3 days post-C2HS during baseline (A) and hypercapnic challenge (B). However, robust return of ipsilateral (IL) EMG was observed by 2 wks and persisted 8 wks post-C2HS. In these examples, there appears to be a modest attenuation of contralateral (CL) intercostal EMG activity in 2 wks and 8 wks rats following an initial robust increase following C2HS.

Fig. 3

The effect of C2HS on rostral intercostal EMG amplitude during baseline breathing and hypercapnic respiratory challenge. Ipsilateral EMG amplitudes during baseline and hypercapnic challenge were expressed relative to the contralateral EMG burst (% CL, A and B). These data indicate that following C2HS the ipsilateral inspiratory EMG burst amplitude was transiently reduced. However, ipsilateral EMG amplitudes recovered by 2 wks post-C2HS. A similar conclusion is reached when examining the EMG amplitude data expressed as arbitrary units (a.u.) (C and D). The C2HS injury caused little change in contralateral intercostal EMG amplitudes compared with uninjured controls (D). ***P < 0.001, **P < 0.01, *P < 0.05 compared to corresponding baseline value for that group; ^#P < 0.05 compared to other groups; ^†P < 0.05 compared to the 1–3 days post-C2HS group.

Fig. 4

Relationship between VT recovery and intercostal EMG bursting following C2HS. A linear regression analysis suggested a strong positive correlation between ipsilateral (IL) EMG activity and recovery of VT (P < 0.001, A). Conversely, no clear relationship exists between contralateral (CL) EMG activity and VT following C2HS (B).