Contrasting properties of pyramidal tract neurons located in the precentral or postcentral areas and of corticorubral neurons in the behaving monkey.
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Biomedical subjects
Publications and source records attributed to C Fromm.
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Recordings with pyramidal tract neurons (PTNs) in the primary somatosensory cortex of the monkey show that these neurons have 3 properties in common with PTNs of primary motor cortex: (1) they exhibit discharge prior to the onset of voluntary movement, (2) their discharge frequency varies as a function of strength of muscular contraction, and (3) they show reflex responses to afferent stimuli that occur during movement. These findings support the view that in addition to its widely recognized role in somesthetic perception, somatosensory cortex has a direct role in the control of movement.
Sherrington proposed that the major role of proprioceptors is in processing afferent inputs generated by the active movements of the animal itself, and noted that the reflex effects of proprioceptive inputs are "mild." Current experimental results are consistent with the view that the major role of both segmental and transcortical proprioceptive reflexes is in small active movements and active postural stability, with muscle afferent inputs reducing "...errors of muscle length produced by fluctuating levels of motor discharge..." as stated by Goodwin and coworkers in 1978. Exteroceptive reflexes generate intense muscular responses and are of critical importance in prompt reprogramming essential for effective responses to environmental stimuli. Within the motor cortex (MI) there is a caudal region (MI/c) which receives exteroceptive cutaneous inputs and a rostral region (MI/r) which receives proprioceptive inputs. Transcortical reflexes mediated via pyramidal tract neurons (PTNs) of MI/r have properties which are analogous to segmental proprioceptive reflexes: changes of muscle length elicit PTN discharges which oppose the length change and so act to maintain stability. Furthermore, MI/r PTNs which are recruited earliest for small active movements are most sensitive to proprioceptive inputs. Data are not yet available concerning transcortical reflexes via MI/c during voluntary movement, but it is speculated that the cutaneous reflexes via MI/c might be functionally analogous to segmental cutaneous reflexes. Short-latency reflex responses also occur in postcentral (PoC) PTNs, and in this report we present results concerning the properties of PoC PTNs during active and passive movement. Caudal (area 2-5) PoC PTNs were similar to MI PTNs in that they often discharged prior to electromyogram (EMG) activity with active movement, and had different discharge frequencies with different steady state loads, but were unlike most MI PTNs in having the same changes of discharge with active and passive movement. Our finding of PoC discharge prior to movement onset, confirming that of Soso and Fetz in 1980, is discussed in connection with the concept of corollary discharge.
Activity of motor cortex pyramidal tract neurons (PTNs) was recorded in monkeys making large (20 degrees), high velocity and small (1 to 2 degrees), low velocity pronation-supination arm movements in a visual pursuit-tracking paradigm. Antidromic response latencies (ADLs) or PTNs were examined in relation to PTN modulation with the large and small movements to test the hypothesis that PTNs would exhibit a "size principle" analogous to that of spinal cord motoneurons. It was found that smaller PTNs (i.e., those having longer ADLs) discharged just as strongly with small, slow movements as with large, fast movements, while about one-third of the larger PTNs (even those selected for a significant relation to small movement) discharged more intensely with the large movement. Another analysis dealing with PTNs in a selected set of penetrations in an area focal for pronation-supination showed that PTNs with longer ADLs (greater than 1 msec) were more likely to reach maximum frequency with small, slow movement. There was, however, much overlap in the behavior of small and large PTNs, and while there was a statistically significant relation between size and movement-related activity of PTNs, there did not seem to be a "size principle" in the strict sense that this term has been used with reference to spinal cord motoneurons.
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The influence of varying the muscular afferent fiber input on both the normal firing rate (Fn) and the amount of recurrent inhibition (Fn-Fi) induced by a constant ventral root stimulation was investigated on tonic extensor motoneurons recorded from ventral root filaments in decerebrate cats. The afferent input was varied by graded electrical stimulation of the gastrocnemius nerves and by vibrating the triceps surae muscle (100 mum amplitude). When the input consisted solely of impulses in Ia afferents, as was the case during vibration, the mean recurrent inhibition Fn-Fi was 2.3 times greater than during nerve tetanization at 1.8 times threshold of group I (TI). This strength generally excited all group I and some low-threshold group II afferents. Between 1.8 TI and 8 TI, Fn-Fi decreased by some 50%. The average Fn increased slightly and motoneurons with a phasic discharge pattern were recruited when the stimulus strength was raised so as to excite group II afferents; these cells were never recruited during vibration and nerve tetanization at 1.8 TI. The results indicate the possibility of a disinhibitory action of secondary muscle spindle afferents on extensor motoneurons by reducing the recurrent inhibition.
About 2/3 of the gamma efferents isolated from the medial gastrocnemius nerve were inhibited by longitudinal high-frequency vibration applied to the tendons of the non-contracting pretibial flexors (decerebrate cats). The inhibition appeared at 15-25 mum amplitude of vibration and increased up to maximum at nearly 100 mum. Increasing the frequency of vibration from 100 to 300 Hz increased the inhibition. The reflex effects elicited by muscle vibration corresponded well in incidence and magnitude with those evoked by tetanization of the deep peroneal nerve at group I stimulus strength. The reflex disappeared when the nerve supply of the vibrated muscles was cut. The sensitivity of some pretibial proprioceptors to vibration was also tested. It is concluded that primary spindle endings of the pretibial flexors inhibit the extensor gamma motoneurons. Some findings hint at a spinal pathway involving Ia inhibitory interneurons. In addition, an inhibitory action of pretibial group II afferents, probably secondary spindle endings, on extensor gamma efferents was demonstrated. The described fusimotor inhibition by antagonistic muscle spindle afferents is a further example of alpha-gamma-linkage.
1. High frequency vibration was applied to the tendon of the non-contracting triceps surae muscle while recording the background discharges of single gamma fibres only small nerve bundles were cut, leaving most of the nerve supply to the triceps intact. 2. 22% out of a total of sixty-three gamma efferents were tonically inhibited by vibration. The inhibition appeared between 25 and 50mum peak-to-peak amplitude of vibration and increased to a plateau for amplitudes of about 100mum. The dependence of the tonic vibration reflex of alpha-efferents on the amplitude of vibration was found to be similar. Increasing the frequency of vibration from 150 to 300 Hz increased the degree of inhibition. 3. 33% of the fusimotor neurones investigated responded to muscle vibration with an increase in discharge rate. The threshold amplitudes of this reflex ranged from 20 to 50mum. Some features of the reflex, in particular the parallel post-vibratory facilitation found in alpha and gamma efferents, pointed to a polysynaptic pathway organized in an alpha-gamma linkage. 4. All gamma efferents inhibited by vibration showed inhibitory responses to antidromic stimulation of the parent ventral root, and most of them were inhibited by ramp stretch of the triceps. The gamma motoneurones facilitated by vibration, however, were excited by muscle stretch and were less susceptible to antidromic inhibition, some lacking it completely. 5. Cutting the nerves to triceps abolished the inhibitory as well as the excitatory responses of gamma efferents to muscle vibration. Both fusimotor reflexes were preserved after spinal section and subsequent administration of L-DOPA. 6. It is concluded that both of the fusimotor reflex effects of vibration are caused by excitation of primary spindle endings within the triceps. The inhibition of fusimotor neurones is thought to be mediated by Renshaw cells activated during vibration. The significance of positive feed-back on to gamma motoneurones as a result of autogenetic facilitation by Ia afferents is discussed in connexion with stability in the stretch reflex loop.
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