Nerve-Specific Input Modulation to Spinal Neurons during a Motor Task in the Monkey

Abstract

If not properly regulated, the large amount of reafferent sensory signals generated by our own movement could destabilize the CNS. We investigated how input from peripheral nerves to spinal cord is modulated during behavior. We chronically stimulated the deep radial nerve (DR; proprioceptive, wrist extensors), the median nerve (M; mixed, wrist flexors and palmar skin) and the superficial radial nerve (SR; cutaneous, hand dorsum) while four monkeys performed a delayed wrist flexion-extension task. Spinal neurons putatively receiving direct sensory input were defined based on their evoked response latency following nerve stimulation. We compared the influence of behavior on the evoked response (responsiveness to a specific peripheral input) and firing rate of 128 neuron-nerve pairs based on their source nerve. Firing rate increased during movement regardless of source nerve, whereas evoked response modulation was strikingly nerve-dependent. In SR ( = 47) and M ( = 27) neurons (cutaneous or mixed input), the evoked response was suppressed during wrist flexion and extension. In contrast, in DR neurons ( = 54, pure proprioceptive input), the evoked response was facilitated exclusively during movements corresponding to the contraction of DR spindle-bearing muscles (i.e., wrist extension). Furthermore, modulations of firing rate and evoked response were uncorrelated in SR and M neurons, whereas they tended to be positively comodulated in DR neurons. Our results suggest that proprioceptive and cutaneous inputs to the spinal cord are modulated differently during voluntary movements, suggesting a refined gating mechanism of sensory signals according to behavior. Voluntary movements produce copious sensory signals, which may overwhelm the CNS if not properly regulated. This regulation is called "gating" and occurs at several levels of the CNS. To evaluate the specificity of sensory gating, we investigated how different sources of somatosensory inputs to the spinal cord were modulated while monkeys performed wrist movements. We recorded activity from spinal neurons that putatively received direct connections from peripheral nerves while stimulating their source nerves, and measured the evoked responses. Whereas cutaneous inputs were suppressed regardless of the type of movement, muscular inputs were specifically facilitated during relevant movements. We conclude that, even at the spinal level, sensory gating is a refined and input-specific process.

Two distinct proprioceptive representations of voluntary movements in primate spinal neurons

“…After excluding from further analysis two neurons that were classified as putative motoneurons, the total number of neurons analyzed was 142. This dataset overlaps with a previous paper (Confais, Kim, Tomatsu, Takei, & Seki, 2017) that focused on the differences between SR and DR neurons (i.e. responsiveness to nerve stimulation, central latency, base firing rate, and intra-spinal depth of each neuron).…”

“…The median of the mean firing rate for five behavioral epochs clearly indicated that the DR and SR neurons increased their activity during active torque (active move and active hold) and passive movement for both flexion and extension movements. Their activity was significantly larger in extension trials (Wilcoxon signed rank test, active move, P = 0.001; active hold, P = 0.020; passive move, P = 0.043) (see also (Confais et al, 2017)). We further characterized this activity by separately counting the number of neurons showing significant modulation relative to rest (Figure 3C) in each behavioral epoch.…”

“…As summarized in Fig. 3, the majority of DR neurons were predominantly active during active extension torque (Confais et al, 2017). This pattern of activity was paradoxical because during extension, extensor muscles (i.e.…”

“…Subsequent histological analysis indicated that this site was located around the border of the dorsal horn and intermediate zone (Takei & Seki, 2010). Considering these data, we speculated that both group of neurons were most likely located in the anterior dorsal horn or the intermediate zone (laminae IV–VII) (Confais et al, 2017), with HFNs and LFNs being intermingled. The segmental latencies and threshold currents to recruit HFNs and LFNs were not significantly different between the two groups (segmental latency, 0.55 ± 0.42 ms (HFNs) and 0.60 ± 0.31 ms (LFNs); threshold current, 1.16 ± 0.22 T (HFNs) and 1.12 ± 0.09 T (LFNs)).…”

“…In addition, as with the other intrinsic properties of these neurons, we compared the putative recording depth of HFNs and LFNs using a method we previously reported (Confais et al, 2017; Takei & Seki, 2010). In short, for each recording track, we considered that the depth of the dorsal edge of the grey matter corresponded to that of the first encountered cell.…”