Heterogenic feedback between hindlimb extensors in the spontaneously locomoting premammillary cat

Abstract

Electrophysiological studies in anesthetized animals have revealed that pathways carrying force information from Golgi tendon organs in antigravity muscles mediate widespread inhibition among other antigravity muscles in the feline hindlimb. More recent evidence in paralyzed or nonparalyzed decerebrate cats has shown that some inhibitory pathways are suppressed and separate excitatory pathways from Golgi tendon organ afferents are opened on the transition from steady force production to locomotor activity. To obtain additional insight into the functions of these pathways during locomotion, we investigated the distribution of force-dependent inhibition and excitation during spontaneous locomotion and during constant force exertion in the premammillary decerebrate cat. We used four servo-controlled stretching devices to apply controlled stretches in various combinations to the gastrocnemius muscles (G), plantaris muscle (PLAN), flexor hallucis longus muscle (FHL), and quadriceps muscles (QUADS) during treadmill stepping and the crossed-extension reflex (XER). We recorded the force responses from the same muscles and were therefore able to evaluate autogenic (intramuscular) and heterogenic (intermuscular) reflexes among this set of muscles. In previous studies using the intercollicular decerebrate cat, heterogenic inhibition among QUADS, G, FHL, and PLAN was bidirectional. During treadmill stepping, heterogenic feedback from QUADS onto G and G onto PLAN and FHL remained inhibitory and was force-dependent. However, heterogenic inhibition from PLAN and FHL onto G, and from G onto QUADS, was weaker than during the XER. We propose that pathways mediating heterogenic inhibition may remain inhibitory under some forms of locomotion on a level surface but that the strengths of these pathways change to result in a proximal to distal gradient of inhibition. The potential contributions of heterogenic inhibition to interjoint coordination and limb stability are discussed.

FIG. 1.

A: oscillations in the background force in quadriceps (QUADS) of the immobilized right hindlimb during stepping. B: ramp-and-hold stretches delivered on top of the oscillating background force in QUADS. →, the force response to a single stretch during stepping.

FIG. 2.

A: recipient muscle stretch-evoked force response during crossed-extension reflex (XER). Symbols above recipient stretches indicate responses obtained when the muscle is stretched alone (•) and together with the donor muscle (▵). B: recipient muscle length input to 2-state stretch. C: donor muscle stretch-evoked force response during XER. D: donor muscle length input for 2-state stretch. A 2-state stretch is performed to ascertain strength and sign of heterogenic feedback between a recipient and donor muscle. The stimulation of the tibial nerve in the left hindlimb at 2 T evokes an increase in the background force of the recipient and donor muscles, flexor hallucis longus (FHL) and gastrocnemius (G) respectively (A and C). As the background force declines, ramp-and-hold stretches (2 mm, 0.04-m/s stretch, 100-ms hold period), are delivered to the recipient and donor muscles (B and D).

FIG. 3.

A: individual force response during XER: background force (i) of an individual stretch is calculated as the average of the force over 10 ms just prior to the ramp and hold stretch; baseline (ii) is calculated for each stretch by performing a linear interpolation between the 1st 10 ms and last 10 ms of data; baseline is subtracted from each individual trace to yield the baseline-subtracted data (iii). B: baseline calculated for an individual stretch despite a shifting background force during stepping.

FIG. 4.

Heterogenic inhibition from G onto FHL, where G is the donor muscle and FHL is the recipient muscle in 1 animal during locomotion with force oscillations for the mechanical phase (A), dynamic phase (B), and static phase (C). • and ▵, FHL force responses from stretches occurring in ramp-and-hold stretch alone (R) and stretching the recipient and donor muscles simultaneously (RD), respectively. Polynomials and 95% confidence intervals are fit to each population of data, and statistical tests reveal that the populations for the dynamic and static phases are distinctly separated (P < 0.01). Two traces matched at 10 N background force in FHL from R (—) and RD (- - -) have been superimposed in the inset of B and C to illustrate the magnitude of inhibition from G onto FHL during locomotion, and the vertical line indicates the sample time. Heterogenic inhibition from G onto FHL is more force-dependent during the dynamic phase than during the static phase. The magnitude of heterogenic inhibition onto FHL for the dynamic and static time points (D) are represented as the difference between polynomials depicted in B and C.

FIG. 5.

A 3-dimensional surface that quantifies the magnitude of heterogenic inhibition from G onto FHL during locomotion as a function of force and time. To quantify the magnitude of heterogenic inhibition from G onto FHL during locomotion, response differences are calculated for every 5 ms over the ramp-and-hold stretch by subtracting the polynomial fits for RD from the polynomial fits from R. A 3-dimensional surface is created from the series of response difference calculations. The heterogenic inhibition from G onto FHL during locomotion remains relatively constant over time and FHL background force.

FIG. 6.

Heterogenic inhibition from G onto plantaris muscle (PLAN), where G is the donor muscle and PLAN is the recipient muscle in 1 animal during locomotion with force oscillations for the mechanical phase (A). B: heterogenic inhibition from G onto PLAN during locomotion for the dynamic phase. C: heterogenic inhibition from G onto PLAN during locomotion for the static phase. The same conventions as Fig. 5 apply. Two traces matched at 10 N background force in PLAN from R (—) and RD (- - -) have been superimposed to illustrate the magnitude of inhibition from G onto PLAN during locomotion, and the vertical line indicates the sample time. Heterogenic inhibition from G onto PLAN during locomotion remains independent of force during the dynamic phase yet increases with increasing force during the static phase. Variability also increases with increasing time. The magnitude of heterogenic inhibition onto PLAN for the dynamic and static time points (D) are represented as the difference between polynomials depicted in B and C.

FIG. 7.

A 3-dimensional surface that quantifies the magnitude of heterogenic inhibition from G onto PLAN during locomotion as a function of force and time. The magnitude of heterogenic inhibition from G onto PLAN during locomotion for the entire time course of the ramp-and-hold stretch was calculated in the same manner as Fig. 6. The heterogenic inhibition from G onto PLAN during locomotion increases slightly over time and remains slightly dependent on PLAN background force at longer latencies.

FIG. 8.

A: heterogenic inhibition from QUADS onto G where QUADS is the donor muscle and G is the recipient muscle in 1 animal during locomotion without force oscillations for the dynamic phase. B: heterogenic inhibition from QUADS onto G during XER for the dynamic phase. The same conventions as Fig. 5 apply. Two traces matched at 6 N (A) and 3.5 N (B) background force from R (—) and RD (- - -) have been superimposed to illustrate the magnitude of inhibition from QUADS onto G during locomotion and XER, respectively, and the vertical line indicates the sample time.

FIG. 9.

A: heterogenic inhibition from FHL onto PLAN, where FHL is the donor muscle and PLAN is the recipient muscle during locomotion without force oscillations for the static phase. B: heterogenic inhibition from FHL onto PLAN during XER for the static phase. Heterogenic inhibition from FHL onto PLAN is similar in strength and sign during locomotion (A) and XER (B). The same conventions as Fig. 5 apply. Matched traces at a background force of 7 N for R (—) and RD (- - -) have been superimposed and inset to demonstrate the trend of heterogenic inhibition in both behavioral states, and the vertical line indicates the sample time.

FIG. 10.

A: heterogenic inhibition from G onto FHL where G is the donor muscle and FHL is the recipient muscle in 1 animal during locomotion with force oscillations for the dynamic phase. B: heterogenic inhibition from G onto FHL during XER for the dynamic phase. Heterogenic inhibition from G onto FHL is similar in strength and sign during locomotion (A) and XER (B). The same conventions as Fig. 5 apply. Matched traces at a background force of 5 N for R (—) and RD (- - -) have been superimposed and inset to demonstrate the trend of heterogenic inhibition in both behavioral states, and the vertical line indicates the sample time.

FIG. 11.

Summary diagram of the heterogenic inhibition among ankle and knee extensors present during locomotion in the spontaneously locomoting premammillary cat and during XER in the intercollicular decerebrate cat. Heterogenic inhibition from G onto PLAN and FHL in the premammillary cat during locomotion remained of similar strength and sign to heterogenic inhibition found in the intercollicular cat during XER, whereas heterogenic inhibition from PLAN or FHL onto G was significantly weaker. - - -, those reflexes that appeared to be modulated between XER and treadmill stepping. The net effect of the modulation was to produce a proximal to distal gradient of inhibition.