Reticulospinal Contributions to Gross Hand Function after Human Spinal Cord Injury

Abstract

Multiple descending motor pathways likely contribute to the recovery of hand motor function following spinal cord injury (SCI). Reticulospinal neurons project to spinal motor neurons controlling hand muscles and extensively sprout into gray matter structures after SCI; therefore, it has been proposed that the reticulospinal tract is one of the descending motor pathways involved in recovery of hand function after injury. To test this hypothesis, we examined the StartReact response, an involuntary release of a planned movement via a startling stimulus that engages the reticulospinal tract, by measuring reaction times from electromyographic activity in an intrinsic finger muscle during three motor tasks requiring different degrees of hand dexterity: index finger abduction, a precision grip, and a power grip. Males and females with and without incomplete chronic cervical SCI were tested. We found that although SCI participants voluntarily responded to all tasks, reaction times were shorter during a startle cue while performing a power grip but not index finger abduction or precision grip. Control subjects had similarly shorter reaction times during a startle cue in all motor tasks. These results provide the first evidence for a contribution of the reticulospinal tract to hand control in humans with SCI during gross finger manipulations and suggest that this contribution is less pronounced during fine dexterous finger movements.SIGNIFICANCE STATEMENT It has been long proposed that brainstem pathways contribute to the recovery of hand function in humans with spinal cord injury (SCI). Here, we show that individuals with anatomically incomplete chronic cervical SCI responded to a startle stimulus, a test that engages the reticulospinal tract, while performing a power grip but not during index finger abduction or precision grip. Control subjects responded to a startle stimulus similarly across tasks. These observations suggest that reticulospinal outputs after SCI contribute to hand motor tasks involving gross finger movements. Interestingly, this contribution is less pronounced during fine dexterous finger movements.

Keywords: corticospinal tract; grasping; hand control; primary motor cortex; tetraplegia; voluntary drive.

Figure 1.

Experimental setup. A, Schematic of the hand postures tested including index finger abduction, a precision grip, and a power grip. B, Representation of the paradigm used to examine the StartReact response in both groups. A red LED was presented alone or in combination with a quiet acoustic stimulus (80 dB; 500 Hz, 20 ms) or a SAS (115 dB; 500 Hz, 20 ms).

Figure 2.

VRT, VART, and SVRT. We measured the VRT (A), VART (B), and VSRT (C) during index finger abduction, precision grip, and power grip in controls and SCI participants. Group data are shown in bar graphs (controls, n = 22; SCI, n = 17). The abscissa shows the hand postures tested in both groups (index finger abduction, white bars; precision grip, light gray bars; power grip, dark gray bars). The ordinate shows the reaction time (in milliseconds). Note that overall, VRT, VART, and VSRT values were larger in SCI compared with control participants. Error bars indicate SE. *p < 0.05.

Figure 3.

ΔT_SR/ΔT_AR ratios. A, Raw EMG data in a representative control (left) and SCI (right) subject showing rectified traces during VRT (black traces), VART (red traces), and VSRT (blue traces). Reaction times were measured during all conditions and arrows below each of the traces indicates the reaction time in each of the conditions tested. The EMG traces were aligned to the cue onset. The cue onset is not shown to zoom in on the reaction time across conditions (see arrows). Note that VSRT was always shorter in all tasks in the control subject, whereas in the SCI subject VSRT was only shorter during the power grip task. B, Group data are shown in bar graphs (controls, n = 22; SCI, n = 17). The abscissa shows the hand postures tested in both groups (index finger abduction, white bars; precision grip, light gray bars; power grip, dark gray bars). The ordinate shows the ΔT_SR/ΔT_AR ratios (see Materials and Methods for a detailed description). Note that in SCI subjects ratios were maintained to a similar level as control subjects during power grip but not during index finger abduction and precision grip. Error bars indicate SE. *p < 0.05, comparison between groups; ¥p < 0.05, comparison between tasks.