Response patterns and postspike effects of premotor neurons in cervical spinal cord of behaving monkeys.
Most of our information about spinal neurons has been derived from experiments with anesthetized or surgically. reduced preparations. To investigate these neurons under normal behavioral conditions, we recorded the activity of single afferent units in cervical dorsal root ganglia and of single interneurons in the cervical spinal cord of macaque monkeys, as they generated alternating flexion and extension torques about the wrist. Spike-triggered averages of rectified electromyographic activity were used to identify "premotor" (PreM) units associated with correlated postspike effects in active muscles. In addition to postspike effects, some spike-triggered averages showed early increases in average muscle activity, which were attributed to synchronous discharges in other PreM units. In recordings of peripheral afferents, 49% of the task-related dorsal root ganglia units produced postspike facilitation (PSF) of at least one forearm muscle, with a mean PSF latency of 5.8 +/- 0.3 ms (SE). The PSF amplitude was measured as the mean percent increase (MPI): the average increase of the PSF as a percentage of the prespike baseline mean. PreM afferent units produced PSF with an average MPI of 4.6 +/- 0.3%. In a study of cervical interneurons, about 13% (72/562) of the task-related cells showed postspike effects. These PreM interneurons had a mean PSF latency of 7.2 +/- 0.3 ms and a mean MPI of 4.6 +/- 0.2%. The MPI values for spinal neurons were similar to the MPIs reported for rubromotoneuronal and corticomotoneuronal cells. PreM neurons usually facilitated a subset of the coactivated muscles called the unit's "muscle field." The PreM afferents facilitated an average of 46% of the synergistically coactivated muscles, while PreM interneurons facilitated an average of 37%. These are comparable with the percentage of muscles facilitated by corticomotoneuronal (40%) and rubromotoneuronal (50%) cells. During the step-tracking task the monkeys generated ramp-and-hold torques about the wrist. The PreM afferents typically became active during either flexion or extension of the wrist, although a few were bidirectionally active. The most common response pattern in PreM afferents was a tonic discharge, followed by phasic and phasic-tonic discharge. The most common patterns exhibited by PreM interneurons were tonic and phasic-tonic responses. PreM afferent units began to discharge on average 51 +/- 13 ms before activation of their target muscle. This early onset supports our hypothesis that these PreM afferents arose from muscle spindles, which is also consistent with their short-latency PSF and their responses to perturbations that stretched their target muscles. The results reveal some salient differences between the discharge properties of dorsal root ganglia neurons, spinal interneurons, and supraspinal PreM cells in the motor cortex and red nucleus. All four PreM populations include tonic, phasic-tonic, and phasic cells, but in significantly different proportions. Most PreM afferents resembled corticomotoneuronal cells in being active only with their target muscles, unlike rubromotoneuronal cells and spinal PreM interneurons, which tended to exhibit more bidirectional discharges.
Fetz
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Department of Physiology and Biophysics, University of Washington, Seattle 98195, USA.
Perlmutter
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Maier
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Flament
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Fortier
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D000344:Afferent Pathways / Q000166:cytology / Q000502:physiology; D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D004576:Electromyography; D004594:Electrophysiology; D005071:Evoked Potentials / Q000502:physiology; D005727:Ganglia, Spinal / Q000166:cytology; D007395:Interneurons / Q000502:physiology; D008251:Macaca; D009046:Motor Neurons / Q000502:physiology*; D018482:Muscle, Skeletal / Q000294:innervation / Q000502:physiology; D011597:Psychomotor Performance / Q000502:physiology; D013116:Spinal Cord / Q000166:cytology / Q000502:physiology*