Heteronymous excitatory feedback from muscle spindles and inhibitory feedback from Golgi tendon organs and recurrent inhibitory circuits can influence motor coordination. The functional role of inhibitory feedback is difficult to determine because nerve stimulation, the primary method used in humans, cannot evoke inhibition without first activating the largest diameter muscle spindle axons. Here, we tested the hypothesis that quadriceps muscle stimulation could be used to examine heteronymous inhibition more selectively when compared to femoral nerve stimulation by comparing the effects of nerve and muscle stimulation onto ongoing soleus EMG held at 20% of maximal effort. Motor threshold and two higher femoral nerve and quadriceps stimulus intensities matched by twitch evoked torque magnitudes were examined. We found that significantly fewer participants exhibited excitation during quadriceps muscle stimulation when compared to nerve stimulation (14–29% vs 64–71% of participants across stimulation intensities) and the magnitude of heteronymous excitation from muscle stimulation, when present, was much reduced compared to nerve stimulation. Muscle and nerve stimulation resulted in heteronymous inhibition that significantly increased with increasing stimulation evoked torque magnitudes. This study provides novel evidence that muscle stimulation may be used to more selectively examine inhibitory heteronymous feedback between muscles in the human lower limb when compared to nerve stimulation.

Force feedback from Golgi tendon organs (GTOs) has widespread intermuscular projections mediated by interneurons that share inputs from muscle spindles, among others. Because current methods to study GTO circuitry (nerve stimulation or muscle stretch) also activate muscle spindle afferents, the selective role of GTOs remains uncertain. Here, we tested the hypothesis that intramuscular stimulation evoked twitch contractions could be used to naturally bias activation of GTOs and thus evaluate their intermuscular effects in decerebrate cats. This was achieved by comparing the effects of twitch contractions and stretches as donor inputs onto the motor output of recipient muscles. Donor–recipient pairs evaluated included those already known in the cat to receive donor excitatory muscle spindle feedback only, inhibitory GTO feedback only, and both excitatory spindle and inhibitory GTO effects. Muscle stretch, but not twitch contractions, evoked excitation onto recipient muscles with muscle spindle afferent inputs only. Both donor muscle stretch and twitch contractions inhibited a recipient muscle with GTO projections only. In a recipient muscle that receives both muscle spindle and GTO projections, donor muscle stretch evoked both excitatory and inhibitory effects, whereas twitch contractions evoked inhibitory effects only. These data support the hypothesis that muscle stimulation evoked contractions can induce intermuscular effects most consistent with mechanical GTO receptor activation and not direct activation of sensory axons. We propose this approach can be used to evaluate GTO circuitry more selectively than muscle stretch or nerve stimulation and can be adapted to study GTO feedback non-invasively in freely moving cats and humans.

Excitatory feedback from muscle spindles, and inhibitory feedback from Golgi tendon organs and recurrent inhibitory circuits are widely distributed within the spinal cord to modulate activity between human lower limb muscles. Heteronymous feedback is most commonly studied in humans by stimulating peripheral nerves, but the unique effect of non-spindle heteronymous feedback is difficult to determine due to the lower threshold of excitatory spindle axons. A few studies suggest stimulation of the muscle belly preferentially elicits non-spindle heteronymous feedback. However, there remains a lack of consensus on the differential effect of nerve and muscle stimulation onto the H-reflex, and the relation of the heteronymous effects onto H-reflex compared to that onto ongoing EMG has not been determined. In this cross-sectional study, we compared excitatory and inhibitory effects from femoral nerve and quadriceps muscle belly stimulation onto soleus H-reflex size in 15 able-bodied participants and in a subset also compared heteronymous effects onto ongoing soleus EMG at 10% and 20% max. Femoral nerve stimulation elicited greater excitation of the H-reflex compared to quadriceps stimulation. The differential effect was also observed onto ongoing soleus EMG at 20% max but not 10%. Femoral nerve and quadriceps stimulation elicited similar inhibition of the soleus H-reflexes, and these results were better associated with soleus EMG at 20%. The results support surface quadriceps muscles stimulation as a method to preferentially study heteronymous inhibition at least in healthy adults. The primary benefit of using muscle stimulation is expected to be in persons with abnormal, prolonged heteronymous excitation. These data further suggest heteronymous feedback should be evaluated with H-reflex or onto ongoing EMG of at least 20% max to identify group differences or modulation of heteronymous feedback in response to treatment or task.

Muscle spindle afferent feedback is modulated during different phases of locomotor tasks in a way that facilitates task goals. However, only a few studies have studied H-reflex modulation during landing. This study aimed to characterize soleus (SOL) H-reflex modulation during the flight and early landing period of drop landings. Since landing presumably involves a massive increase in spindle afferent firing due to rapid SOL muscle stretching, we hypothesized H-reflex size would decrease near landing reflecting neural modulation to prevent excessive motoneuron excitation. The soleus H-reflex was recorded during drop landings from a 30 cm height in nine healthy adults. Electromyography (SOL, tibialis anterior (TA), medial gastrocnemius, and vastus lateralis), ankle and knee joint motion and ground reaction force were recorded during landings. Tibial nerve stimulation was timed to elicit H-reflexes during the flight and early ground contact period (five 30 ms Bins from 90 ms before to 60 ms after landing). The H-reflexes recorded after landing (0–30 and 30–60 ms) were significantly smaller (21–36% less) than that recorded during the flight periods (90–0 ms before ground contact; P ≤ 0.004). The decrease in H-reflex size not occurring until after ground contact indicates a time-critical modulation of reflex gain during the last 30 ms of flight (i.e., time of tibial nerve stimulation). H-reflex size reduction after ground contact supports a probable neural strategy to prevent excessive reflex-mediated muscle activation and thereby facilitates appropriate musculotendon and joint stiffness.

Inhibitory pathways from Golgi tendon organs project widely between muscles crossing different joints and axes of rotation. Evidence suggests that the strength and distribution of this intermuscular inhibition is dependent on motor task and corresponding signals from the brainstem. The purpose of the present study was to investigate whether this sensory network is altered after spinal cord hemisection as a potential explanation for motor deficits observed after spinal cord injury (SCI). Force feedback was assessed between the long toe flexor and ankle plantarflexor (flexor hallucis longus), and the three major ankle extensors, (combined gastrocnemius, soleus, and plantaris muscles) in the hind limbs of unanesthetized, decerebrate, female cats. Data were collected from animals with intact spinal cords (control) and lateral spinal hemisections (LSHs) including chronic LSH (4–20 weeks), subchronic LSH (2 weeks), and acute LSH. Muscles were stretched individually and in pairwise combinations to measure intermuscular feedback between the toe flexor and each of the ankle extensors. In control animals, three patterns were observed (balanced inhibition between toe flexor and ankle extensors, stronger inhibition from toe flexor to ankle extensor, and vice versa). Following spinal hemisection, only strong inhibition from toe flexors onto ankle extensors was observed independent of survival time. The results suggest immediate and permanent reorganization of force feedback in the injured spinal cord. The altered strength and distribution of force feedback after SCI may be an important future target for rehabilitation.