Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching.
Neuronal activity was recorded from the superior colliculus (SC) and the underlying reticular formation in two monkeys during an arm reaching task. Of 744 neurons recorded, 389 (52%) clearly modulated their activity with arm movements. The temporal activity patterns of arm-movement-related neurons often had a time course similar to rectified electromyograms (EMGs) of particular muscles recorded from the shoulder, arm or trunk. These reach cells, as well as the muscles investigated, commonly exhibited mono- or biphasic (less frequently tri- or polyphasic) excitatory bursts of activity, which were related to the (pre-)movement period, the contact phase and/or the return movement. The vast majority of reach cells exhibited a consistent activity pattern from trial to trial as did most of the muscles of the shoulder, arm and trunk. Similarities between the activity patterns of the neurons and the muscles were sometimes very strong and were especially notable with the muscles of the shoulder girdle (e.g. trapezius descendens, supraspinatus, infraspinatus or the anterior and medial deltoids). This high degree of co-activation suggests a functional linkage, though not direct, between the collicular reach cells and these muscles. Neuronal activity onset was compared with that of 25 muscles of the arms, shoulders and trunk. The majority of cells (78.5%) started before movement onset with a mean lead time of 149+/-90 ms, and 36.5% were active even before the earliest EMG onset. The neurons exhibited the same high degree of correlation (r=0.97, Spearman rank) between activity onset and the beginning of the arm movement as did the muscles (r=0.98) involved in the task. The mean neuronal reach activity (background subtracted) ranged between 7 and 193 impulses/s (mean 40.5+/-24.2). The mean modulation index calculated [(reach activity background activity)/reach activity+background activity)] was 0.75+/-0.23 for neurons (n=358) and 0.87+/-0.14 for muscles (n=25). As the monkeys fixated the reach target constantly during an arm movement, neuronal activity which was modulated in this period was not related to eye movements. The three neck muscles investigated in the reach task exhibited no reach-related activity modulation comparable to that of either the reach cells or the muscles of the shoulder, arm and trunk. However, tonic neck muscle EMG was monotonically related to horizontal eye position. The clear skeletomotor discharge characteristics of arm-movement-related SC neurons revealed in this study agree with those already known from other sensorimotor regions (for example the primary motor, the premotor and parietal cortex, the basal ganglia or the cerebellum) and are consistent with the possible role of this population of reach cells in the control of arm movements.
Werner
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W
Department of Zoology and Neurobiology, Ruhr University of Bochum, Germany.
Dannenberg
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S
Hoffmann
K P
KP
D000818:Animals; D001132:Arm / Q000294:innervation / Q000502:physiology*; D003216:Conditioning, Operant / Q000502:physiology; D004567:Electrodes, Implanted; D004576:Electromyography; D005073:Evoked Potentials, Somatosensory / Q000502:physiology; D005133:Eye Movements / Q000502:physiology; D007839:Functional Laterality / Q000502:physiology; D008253:Macaca mulatta; D009046:Motor Neurons / Q000502:physiology*; D009068:Movement / Q000502:physiology*; D018482:Muscle, Skeletal / Q000294:innervation / Q000502:physiology*; D009334:Neck Muscles / Q000294:innervation / Q000502:physiology; D011930:Reaction Time / Q000502:physiology; D012154:Reticular Formation / Q000166:cytology / Q000502:physiology*; D012782:Shoulder / Q000502:physiology; D013477:Superior Colliculi / Q000166:cytology / Q000502:physiology*; D013909:Thorax / Q000502:physiology