Proprioceptive control of extensor activity during fictive scratching and weight support compared to fictive locomotion

Abstract

At rest, extensor group I afferents produce oligosynaptic inhibition of extensor motoneurons. During locomotor activity, however, such inhibition is replaced by oligosynaptic excitation. Oligosynaptic excitation from extensor group I afferents plays a crucial role in the regulation of extensor activity during walking. In this study we investigate the possibility that this mechanism also regulates extensor muscle activity during other motor tasks. We show that the reflex pathways responsible for extensor group I oligosynaptic excitation during fictive locomotion can be activated during both fictive scratching and fictive weight support (tonic motor activity induced by contralateral scratching). These observations suggest that the excitatory group I oligosynaptic reflex pathways are open for transmission during several forms of motor activities. We also show that extensor group I input during fictive scratching can affect the amplitude and the timing of extensor activity in a pattern similar to that observed during locomotion. Most likely these effects involve the activation of the excitatory group I oligosynaptic reflex pathways. Accordingly, it is suggested that extensor group I oligosynaptic excitation during motor activities other than locomotion is also used to regulate extensor muscle activity. Furthermore, the similarity of effects from extensor group I input on the rhythmicity during scratching and locomotion supports the hypothesis that both rhythms are generated by a common network.

Fig. 1.

Motoneuronal activities during fictive scratching and weight support. Top to bottom,intracellular recording from an SmAB motoneuron (top trace), ENG recordings from the left hindlimb extensor (SmAB), flexor (Sart, TA), and hip extensor/knee flexor (PBSt) nerves (middle four traces) and ENG recordings from the right hindlimb extensor (Pl) and flexor (DP) nerves (bottom two traces). A, Fictive scratching was induced by manual stimulation of the left pinna and monitored with both intracellular recording from an extensor motoneuron in the left spinal cord (insert) and ENG recordings from left hindlimb nerves. Fictive scratching consisted of two periods: (1) an initial approach period during which extensor motoneurons (SmAB) were tonically hyperpolarized and hip, knee, and ankle flexor nerves (Sart,TA) fired tonically, and (2) a rhythmic period during which the bursts of activity in hip (SmAB, PBSt) and ankle extensors (MG, LGS; data not shown) alternated with bursts in hip (Sart) and ankle (TA) flexors. In the right hindlimb, sustained activity was seen in Pl extensor nerve (arrow). B, Fictive weight support was induced by stimulation of the right pinna so it could be monitored with the same intracellular and left hindlimb ENG recordings as inA. The tonic increase in extensor activity during fictive weight support was generally more pronounced in hip (SmAB and PBSt) than in ankle extensors (data not shown). The intracellular record during fictive weight support shows that sustained depolarization of the extensor motoneuron was accompanied by small, cyclic reductions in membrane potential as rhythmic scratching activity appeared in the right hindlimb extensors. In both panels, the vertical bars below the intracellular waveform indicate single shock stimulation to LGS nerve.

Fig. 2.

Ankle extensor group I afferents evoke disynaptic EPSPs not only during fictive locomotion but also during fictive scratching and weight support. The top two traces in A–C are averaged intracellular recordings from an MG motoneuron, showing the group I disynaptic excitatory response (hatched areas) evoked by MG nerve stimulation during fictive locomotion, scratching, and weight support. During locomotion (A) and scratching (B), the superimposed traces are the averages during extension (solid trace) and flexion (dotted trace). In C, superimposed traces are from the averages during weight support (solid trace) and at rest (dotted trace). In all panels, the middle trace is the arithmetic difference between the top two traces. The bottom trace is the cord dorsum potential record of the arrival of the afferent volley (vertical dashed line). Number of trials used in the calculation of the averages and the value of the membrane potential are indicated.

Fig. 3.

Modulation of group I polysynaptic EPSPs during fictive locomotion, scratching, and weight support. Averaged intracellular recordings from three different motoneurons (1 MG and 2 LGS) showing polysynaptic group I EPSPs (hatched areas) evoked by ankle extensor stimulation during fictive locomotion (A), scratching (B), and weight support (C). Note that when the stimulation was applied during the extension phase of either locomotion or scratching, or during weight support, disynaptic group I EPSPs were also evoked (arrows). For other details, see Figure2.

Fig. 4.

Mean latency and amplitude of disynaptic and polysynaptic group I EPSPs during fictive locomotion, scratching, and weight support. The mean latency and amplitude during fictive locomotion, scratching, and weight support are shown both for the disynaptic (A_1,A₂) and the polysynaptic group I EPSPs (B_1, B₂). The values during the different phases of locomotion and scratching are indicated separately. The means (open circles) are shown with their corresponding SEs (rectangular boxes). SDs are also displayed (vertical bars). Theasterisks indicate single observation.

Fig. 5.

Continuous activation of ankle extensor group I afferents increases the frequency of the scratching rhythm.A, Pl nerve was stimulated continuously for ∼3 sec during scratching. B, The averages during (n = 18; solid trace) and in the absence (n = 18; dashed trace) of stimulation showing that bursts in SmAB were increased both in amplitude and duration whereas the bursts in Sart were increased in amplitude but reduced in duration. After the stimulation, the bursts in SmAB and Sart returned to their original duration (C andD). Similar effects were seen when continuous stimulation was applied again (second stimulation). During stimulations, the majority of the individual scratching cycle durations were reduced (E). At cessation of stimulations, the rhythm frequency returned to a lower value.

Fig. 6.

Activation of ankle extensor group I afferents resets the scratching rhythm. Short trains to the Pl nerve were given during the flexion phase of scratching (1.8 T × 20; 300 Hz). A small bout of the recording session with integrated, rectified ENGs from Sart and SmAB nerves is displayed in A. The normalized averages (B) were from eight stimulated (solid trace) and 31 control (dashed trace) cycles. C, The effect of Pl nerve stimulation on the scratching cycle duration for the whole recording session is shown. Stimulated cycles are represented by solid circles (arrow).

Fig. 7.

Ankle extensor group I input prolongs the activity of extensors. A, Pl nerve stimulation (trains of 10 stimuli, 200 Hz) was given during the extension phase of scratching.B, The corresponding normalized averages showing that Pl stimulation increased the duration of SmAB burst and prolonged the silent period in Sart. The effects of the stimulation on the duration of SmAB activity and the scratching cycle for the whole recording session (three bouts of scratching) are shown in C andD, respectively.