J. F. Iles

Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb.

1. Presynaptic inhibition of soleus muscle Ia afferent fibres, produced by stimulation of group I afferents in the common peroneal nerve, was assessed from changes in the H reflex at long conditioning intervals, in six normal subjects. 2. Stimulation of the ipsilateral sural nerve at the malleolus, just before stimulation of the common peroneal nerve at the head of the fibula, decreased the presynaptic inhibition. This effect was strongest during voluntary plantar flexion and weaker during dorsiflexion or at rest. 3. Stimulation of other cutaneous nerve branches serving the dorsum of the ipsilateral foot, and also the contralateral sural nerve, decreased presynaptic inhibition. Adequate stimulation of low threshold cutaneous mechanoreceptors by light brushing of both distal dorsal and plantar surfaces of the ipsilateral foot decreased presynaptic inhibition. 4. Stimulation of the ipsilateral plantar nerves increased presynaptic inhibition, but this action is attributed to activation of group I afferents from the intrinsic muscles of the foot. 5. Transcranial magnetic stimulation of the lower limb area of the contralateral motor cortex decreased presynaptic inhibition. This effect was strongest during voluntary plantar flexion and weaker during dorsiflexion or at rest. 6. The actions of cutaneous and corticospinal pathways completely occluded each other. However, when both effects were adjusted to be liminal, a spatial facilitation between them was observed. 7. It is concluded that in man, as in the cat, cutaneous and corticospinal axons converge on interneurones that inhibit the machinery of presynaptic inhibition of group Ia afferents. These actions may be responsible for the modulation of presynaptic inhibition which has been observed to precede and accompany a wide range of human movements.

Inhibition of monosynaptic reflexes in the human lower limb.

1. Presynaptic inhibition of muscle spindle Ia afferents by afferents from the same and other muscles has been studied in the human lower limb. The experiments have utilized conditioning of test monosynaptic reflexes by vibration of both the test and other muscles. 2. The pattern of inhibition invariably includes autogenetic actions. 3. There are powerful effects from flexor to extensor Ia afferents. Actions from flexor to flexor, and from extensor to extensor, are weaker. Actions from extensors to flexors are very weak. 4. The strength of presynaptic inhibition from one muscle type to another weakens as the muscles considered become more anatomically distant. 5. The inhibition studied both by vibration and by electrical conditioning stimulation of nerves becomes weaker during voluntary isometric contraction of the test muscle. It is strongest at rest and during antagonist contraction. 6. Evidence is provided suggesting that descending control is the primary cause of this modulation of inhibition during contraction. 7. Stimulation of afferents in cutaneous nerves reduces group I presynaptic inhibition of Ia afferents.

Cortical modulation of transmission in spinal reflex pathways of man.

1. The motor actions in the lower limb of transcranial electrical stimulation of the motor cortex have been studied in sitting human subjects. 2. Cortical stimulation induced a short latency inhibition of H reflexes evoked in soleus motoneurones both at rest and during small voluntary contractions of soleus. 3. Spatial interaction between cortical inhibition of soleus motoneurons and inhibition evoked through identified spinal reflex machinery was investigated. 4. Interactions were found between cortically evoked inhibition and spinal Ia reciprocal inhibition, group I non‐reciprocal inhibition and higher threshold components of longer latency reciprocal inhibition (D1 and D2 inhibitions). 5. Interactions were facilitatory when cortical and spinal inhibitory actions were weak and reversed to occlusion when both actions were strong. 6. It is concluded that the corticospinal pathway converges on the interneurones which subserve Ia reciprocal, group I non‐reciprocal, D1 and D2 inhibition of soleus motoneurones. 7. No significant interaction was found under the present experimental conditions between cortical stimulation and group Ia‐Ia presynaptic inhibition of soleus afferents. 8. The statistical significance of spatial interactions observed with H reflex conditioning was investigated using a control experiment.

Reciprocal inhibition during agonist and antagonist contraction.

SummaryReciprocal inhibition of soleus motoneurones in man was studied during voluntary contraction of soleus or its antagonist. Inhibition was strongest during antagonist contraction or at rest and weak during contraction of soleus itself. Possible explanations for these changes are discussed.

Vestibular-evoked postural reactions in man and modulation of transmission in spinal reflex pathways.

1. The effects of galvanic stimulation of the vestibular apparatus (with electrodes on the mastoid processes) have been studied in standing human subjects. With the head turned to one side, subjects swayed towards the anode. 2. Forwards sway was preceded by electromyographic (EMG) activity in quadriceps and tibialis anterior muscles. Backwards sway was preceded by EMG activity in soleus and hamstring muscles. 3. Using the method of H reflex conditioning, forward sway was found to be preceded by inhibition of soleus motoneurones. 4. Interaction between the vestibular‐evoked inhibition of soleus motoneurones preceding forwards sway and peripheral reflex inhibition was examined by a spatial facilitation method. 5. Interaction was found between vestibular‐evoked inhibition and Ia reciprocal, group I non‐reciprocal and group Ia‐Ia presynaptic inhibitory pathways. It is concluded that vestibular signals converge on spinal interneurones subserving these inhibitory actions. 6. A ‘decoupling’ of soleus motoneurons and soleus‐coupled Renshaw cells was found in the period of soleus activation preceding backwards sway.

Vestibular actions on back and lower limb muscles during postural tasks in man

The vestibular system was activated by galvanic electrical stimulation in 19 normal subjects. With the head turned to one side so that the stimulating anode was on the posterior mastoid process, stimulation caused standing subjects to sway backwards in the sagittal plane. Electromyography showed bilateral activation of erector spinae, gluteus maximus, biceps femoris, soleus and intrinsic foot (toe flexor) muscles. When head direction or electrode polarity was reversed so that the anode was anterior, all those muscles became less active and the subjects swayed forwards. With the head facing forward, stimulation caused sideways sway in the coronal plane, towards the anode, with excitation of the erector spinae on the anode side and reduced activity on the cathode side. The limb muscles were activated on the side opposite the anode and showed complex responses on the anode side. Responses were detectable in the erectores spinae muscles in sitting subjects. No responses in limb muscles were detected in the sitting posture. Subject responses in erector spinae recorded at L3/L4 had latencies from 59 to 110 ms, using a 2 mA stimulus. Latencies in lower limb muscles were longer. The results suggest a role for the vestibular system and descending brain stem motor pathways to the erectores spinae muscles in the control of postural orientation of the back when sitting and standing. The conduction velocity in the motor pathway was estimated to be 13 ± 10 m s−1 (mean ±s.d., n= 12 subjects).

Human standing and walking : comparison of the effects of stimulation of the vestibular system

The adoption of bipedalism by hominids including man has complicated the tasks of balance control and the minimisation of body sway. We have investigated the role of the vestibular organs in controlling sway in the roll direction using galvanic vestibular stimulation (GVS). Two stance conditions were studied: during forward lean posterior compartment muscles are activated and during backward lean anterior compartment muscles are activated. GVS-evoked vestibular signals in stance control leg muscles as a group: all the active muscles in the leg on the GVS cathode side are excited together and those in the contralateral leg (anode side) relax. The subject sways towards the anode side. During treadmill walking, vestibular actions are subtly different: the actions are largely restricted to muscles acting at the ankle joint, occur at longer latencies, are not reciprocal in the opposite limb, are modulated throughout the step cycle (largest early in stance) and are reversed in sign in the peroneus longus muscle. The subject deviates towards the anode side. Hand contact with a firm object reduces GVS-evoked responses in leg muscles during treadmill walking. Responses to GVS are observed during over-ground walking but not significantly during bicycling on an ergometer. The observations suggest that these vestibular actions are part of a roll stabilisation mechanism. They may be mediated through different spinal premotor mechanisms during standing and walking and turned off during bicycling, when leg muscles have no balance control function.

Fictive locomotion in the adult decerebrate rat.

In adult immobilised, decerebrate rats, administration of l-3,4-dihydroxyphenylalanine, stimulation of the mesencephalic locomotor centre, or a combination of the two elicited fictive locomotor patterns in hindlimb muscle nerves. The patterns correspond closely to those observed in decerebrate animals that were free to move.

The speed of passive dendritic conduction of synaptic potentials in a model motoneurone

The time taken for synaptic potentials to spread from a dendritic synapse to the soma of a motoneurone has been calculated. For synapses located on distal parts of the dendritic tree this electrotonic delay can be a large fraction of the total latency of monosynaptic potentials in the cat spinal cord. A method for estimating electrotonic delay from the shape of an individual postsynaptic potential is presented.

Seeking functions for spinal recurrent inhibition

In this issue of The Journal of Physiology, Lamy et al. (2008) describe a rhythmic modulation of recurrent inhibition during walking in man. This provides some insight into the function of recurrent inhibition, first described by Renshaw (1941) as an inhibition of cat motoneurones produced by antidromic stimulation of the axons of neighbouring motoneurones (homonymous action). Subsequent work, also in cats, showed that motor axon collaterals activate interneurones (the eponymous Renshaw cells) that in turn inhibit motoneurones. Actions extend to more distant muscle groups (heteronymous) and parallel the pattern of heteronymous monosynaptic excitation from muscle spindle Ia afferents. Renshaw cells receive peripheral sensory and descending inputs and have output connections to other spinal interneurones and to other Renshaw cells. So recurrent inhibition is more than just negative feedback from and to motoneurones and may have several functions depending upon motor context. Lamy et al. have focused on heteronymous actions (which are more widespread in man than in cats or monkeys) in the context of our unique bipedal form of walking. The knee extensor quadriceps is a source of recurrent inhibition to the ankle extensor and the flexor muscles soleus and tibialis anterior. But given that these ankle muscles are antagonists, how is differential activation achieved? The authors found that around heel strike and early in stance, when quadriceps is active and soleus activity is increasing, recurrent inhibition of soleus is weak. Conversely, later in stance, when quadriceps is active and soleus activity is declining, recurrent inhibition of soleus is strong. Recurrent inhibition of tibialis anterior motoneurones was neither task nor phase dependent. The reduction in soleus recurrent inhibition would assist the transition from swing to stance and enhanced inhibition later in stance would favour the transition from stance to swing by reducing reciprocal inhibition of tibialis anterior. The origin of these changes in recurrent inhibition remains uncertain but activity of peripheral sensory or descending motor pathways could be involved. Two interesting possibilities are the corticospinal pathway, known to depress homonymous recurrent inhibition of soleus in sitting subjects (Mazzocchio et al. 1994) and the vestibulospinal pathway that depresses recurrent inhibition of soleus in standing stance (Iles & Pisini, 1992). It might be possible to extend such studies to heteronymous actions in walking stance. More meticulous experiments built upon the framework of human research protocols pioneered by the Paris group will likely increase our understanding of recurrent inhibition even further.