Influence of aging and task-related activation on descending cortical modulation of spinal sensorimotor circuitry

Abstract

The objective of this study was to evaluate the effects of aging on descending modulation of spinal reflexes across different task conditions. In healthy young (YA; age 27 ± 4 years) and older (OA; age 63 ± 10 years) adults, we utilized paired subthreshold transcranial magnetic stimulation (TMS) and peripheral nerve stimulation (PNS) to elicit unconditioned (PNS only) and conditioned (TMS paired with PNS) soleus Hoffmann (H-)reflexes at 3 inter-stimulus intervals (ISIs) (-1.5, +10 ms, +40 ms) and during 3 task conditions - sit rest (SR), sit active (SA), and quiet stance (QS). Our results showed that at the + 40 ms ISI, compared to YA, the OA group showed significant differences in modulation (and reversal from facilitation to inhibition) of soleus H-reflexes during both SA and QS tasks (p < 0.0001). Correlation analysis showed a significant negative relationship between age and the magnitude of H-reflex modulation at the + 40 ms ISI, such that older individuals showed a larger magnitude of H-reflex inhibition. In conclusion, altered task-related modulation of spinal reflexes at the + 40 ms ISI may reflect specific aging-related effects on spinal sensorimotor integration, likely mediated via complex interactions between the influence of polysynaptic slower-conducting descending pathways, sensory afferents, and local spinal circuits, on spinal reflex activity during motor task performance.

Keywords: Aging; Hoffmann (H-)reflex; Spinal sensorimotor circuitry; Task activation; Transcranial magnetic stimulation (TMS).

Fig. 1

Representative H-reflex traces from a young adult (YA) (left) and older adult (OA) (right) participant, respectively, during each task condition (sit rest, sit active, quiet stance) and at the three inter-stimulus intervals, or ISIs (−1.5 ms, +10 ms, +40 ms). Following the stimulus artifact, in each trace, the dashed black lines (YA) and dashed gray lines (OA) depict unconditioned (UC) H-reflex responses, while the solid, colored lines depict the conditioned H-reflex responses at each of the 3 ISIs (−1.5 ms = blue; +10 ms = red; +40 ms = purple). Note the slightly larger amplitude of the conditioned versus unconditioned H-reflex at the −1.5 ms ISI. At the + 10 ms ISI, the conditioned H-reflex is much larger than the unconditioned H-reflex, consistent with a large % modulation. At the + 40 ms ISI, in OA, compared to unconditioned H-reflexes, the conditioned H-reflex amplitude shows a decrease during task-related activation (sit active and quiet stance). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 2

Conditioned H-reflex % at each ISI during the sit rest (SR) task condition. During SR task condition, both young adult (YA) and older adult (OA) groups showed significantly greater magnitude of Conditioned H-reflex % at the + 10 ms ISI compared to the −1.5 ms ISI (p < 0.0001) and the + 40 ms ISI (p < 0.0001). Error bars depict standard error of the mean. Additionally, the Conditioned H-reflex % at the 40 ms ISI was significantly greater than the −1.5 ms ISI (p = 0.027). *p < 0.05; ****p < 0.0001.

Fig. 3

Conditioned H-reflex % at the −1.5 ms and + 10 ms ISI during three task conditions (SR, SA, QS). (A) At the −1.5 ms ISI (direct, faster), the Conditioned H-reflex % was significantly greater during SA (p = 0.009) and QS (p < 0.0001) compared to SR. (B) At the + 10 ms ISI (indirect, slower), the Conditioned H-reflex % was significantly less during SA (p < 0.001) and QS (p = 0.007) compared to SR. **p < 0.01; ***p < 0.001; ****p < 0.0001. Error bars depict standard error of the mean.

Fig. 4

Conditioned H-reflex % at the + 40 ms ISI during all three task conditions for both young adult (YA) and older adult (OA) groups. (A) Individual data points at the + 40 ms ISI (late indirect) for both YA and OA groups with the Conditioned H-reflex % on the y-axis and the three task conditions on the x-axis. (B) When compared to YA, OA showed significantly lower Conditioned H-reflex % at the + 40 ms ISI during the sit active (SA) (p < 0.0001) and quiet stance (QS) (p < 0.0001) task conditions. No significant difference was observed during sit rest (SR). (C) Within the OA group, the magnitude of Conditioned H-reflex % was significantly reduced during the sit active (SA) (p = 0.0002) and quiet stance (QS) (p = 0.0004) compared to the sit rest (SR) task condition. No significant differences were observed within the YA group. (D) When plotting the Conditioned H-reflex % as a function of age in years, a significant negative correlation was observed for the OA group, where the greater the age of an individual, the more reduced the Conditioned H-reflex % becomes. *p < 0.05; ***p < 0.001; ****p < 0.0001. Error bars depict standard error of the mean.

Fig. 5

The change (Δ) Conditioned H-reflex % between task-related activation conditions (sit active (SA), quiet stance (QS)) versus sit rest (SR)) at each ISI, where the line at 0 indicates no change in the Conditioned H-reflex % between the task conditions. (A) Data for change from sit active (SA) to sit rest (SR) indicate that voluntary activation significantly decreased the magnitude of Conditioned H-reflex % at the + 10 ms (p < 0.0001) and + 40 ms (p < 0.0001) ISIs compared to the −1.5 ms ISI. Additionally, at the + 40 ms ISI, OA showed a greater decrease in the magnitude of Conditioned H-reflex % during voluntary activation compared to YA (p < 0.01). (B) Data for the change from quiet stance (QS) to sit rest (SR) indicate that postural activation significantly decreased the magnitude of Conditioned H-reflex % at the + 10 ms (p < 0.001) and + 40 ms (p < 0.0001) ISIs compared to the −1.5 ms ISI. *p < 0.05; ***p < 0.001; ****p < 0.0001.

Fig. 6

Dynamic balance ability assessed via the narrowing beam walking test (NBWT) and the relation to Conditioned H-reflex % during task-related activation at the + 40 ms ISI. (A) The YA group performed significantly better on the NBWT assessment compared to the OA group (p < 0.0001). (B) Pearson correlation analyses revealed that at the + 40 ms ISI, both YA and OA groups showed no relationship between Conditioned H-reflex (%) and NBWT Score during task-related activation (i.e., SA and QS). Error bars depict standard error of the mean.