Movement-related inputs to intermediate cerebellum of the monkey

P. L E Van Kan, A. R. Gibson, J. C. Houk

Research output: Contribution to journalArticlepeer-review

176 Scopus citations

Abstract

1. The primary goal of this study was to characterize the information about single-joint forelimb movements supplied to intermediate cerebellar cortex by mossy fibers. Discharge of mossy fibers and Golgi cells was studied while monkeys operated six devices that required movements about specific joints. Additional control experiments in anesthetized cats and monkeys established criteria for identification of mossy fibers and Golgi cells. 2. The control experiments demonstrate that mossy fibers can be distinguished from Purkinje and Golgi cells by the waveshapes of their action potentials. Asynaptic activation from the inferior cerebellar peduncle, in combination with histological localization of recording sites in granular layer or subcortical white matter, verified that mossy fibers produce a variety of waveshapes that are characterized by brief initial phases and relatively small amplitudes. The same waveshapes were observed for the mossy fiber recordings from awake monkeys, and many identified mossy fibers had sensory properties similar to those found in the awake animals. From these combined criteria, we conclude that the recordings in the awake animals were from mossy fibers. Golgi cells, recorded exclusively in the granular layer of cerebellar cortex, were characterized by action potentials of longer duration and larger amplitude as compared with mossy fibers, and none were asynaptically activated from the inferior cerebellar peduncle. 3. Units were isolated while the monkeys made free-form and tracking movements. We studied movement-related discharge of 80 mossy fibers and 12 Golgi cells. Mossy fibers showed high modulations during use of at least one of the six manipulanda and had clear preferences for movement about a specific joint, although they often showed consistent but weaker firing during movement about a neighboring joint. Separation of movements by more than one joint produced a large reduction in discharge: shoulder units never fired well to movements of the finger, and finger units never fired well to movement of the shoulder. 4. The tracking task required maintenance of fixed limb positions (a static phase) as well as movements between these positions (a dynamic phase). Of 80 mossy fibers, 18% had purely tonic discharge patterns, 63% were phasic- tonic, and 20% were purely phasic. Discharge patterns were reciprocal (45%), bidirectional (42%), or unidirectional (13%). 5. Eighty percent of the mossy fibers exhibited tonic discharge that was significantly (P < 0.01) correlated with joint angle (r = 0.65 ± 0.19, mean ± SD), and about one third had phasic components that were significantly correlated with movement velocity. Eleven mossy fibers were tested for correlations between the duration of the phasic discharge component and movement duration, and all revealed significant positive correlations. The onset time of mossy fiber discharge was distributed approximately equally about the onset time of movement. Thus discharge of about one fourth of 80 units significantly (P < 0.05) led movement onset and one third significantly lagged. 6. Twenty-nine movement- related mossy fibers were tested for sensory responsiveness by manipulation of joints and/or by mechanical disturbances of device position during static phases of the tracking task. In most (69%) cases, passive responses were of the same polarity as the modulations in discharge during comparable active movements; in 17% of the cases, they were of opposite polarity. Four units (14%) failed to respond to passive movement. 7. Recordings from 12 Golgi cells revealed properties strikingly different from mossy fibers. All showed phasic discharge without tonic components, and most cells showed bidirectional discharge patterns during both active and passive movements. Four of six cells showed modulations in discharge of equal magnitude during use of proximal and distal devices. These properties are consistent with extensive convergence of mossy fibers on individual Golgi cells. 8. It is clear from our results that mossy fibers provide intermediate cerebellum with position, velocity, and direction information about movement of individual forelimb joints. Several characteristics of the signals indicate that they may contain information derived from efference as well as afference. 9. A comparison of input information supplied by mossy fibers with output signals in the nucleus interpositus suggests that the intermediate cerebellum incorporates position and velocity information from individual joints, together with other inputs, into phasic signals relating to coordinated movements of the entire limb.

Original languageEnglish (US)
Pages (from-to)74-94
Number of pages21
JournalJournal of neurophysiology
Volume69
Issue number1
DOIs
StatePublished - 1993

ASJC Scopus subject areas

  • Neuroscience(all)
  • Physiology

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