Movement-related inputs to intermediate cerebellum of the monkey

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.(ABSTRACT TRUNCATED AT 400 WORDS)

Characteristics of Responses of Golgi Cells and Mossy Fibers to Eye Saccades and Saccadic Adaptation Recorded from the Posterior Vermis of the Cerebellum

“…Previous recordings from the OMV and the flocculus during eye movements in monkeys are in accordance with our results about the different patterns of activity recorded from MFs (Kase et al, 1980;Miles et al, 1980;Ohtsuka and Noda, 1992). Similarly, recordings from monkeys in the intermediate cerebellar cortex during forelimb manipulations (van Kan et al, 1993) describe various combinations of tonic and phasic discharges of MFs. In the case of the OMV, the MF afferents have been shown to arise mainly in the pontine nuclei, the nucleus reticularis tegmentis pontis (NRTP), and the paramedian pontine reticular formation (PPRF), suggesting that the cerebellum is provided by both cortical and subcortical information about visually guided eye movements (Thielert and Thier, 1993).…”

“…Whereas the molecular layer remained relatively silent, saccade-related multiunit activity often dominated the background of the granular layer. These criteria are in line with previous electrophysiological identification of cerebellar layers confirmed by histological verification of electrolytic lesion sites in monkeys (Miles et al, 1980;van Kan et al 1993). …”

“…3D). van Kan et al (1993) furthermore confirmed this identification by asynaptic activation of such units from electrical stimuli of the peduncle. We excluded GrCs as the possible origin of such potentials because the size of their somata (4 -6 m) seems to be much smaller than that of MF rosettes, which makes their recording possible only if high impedance electrodes (Ͼ15 M⍀) are used (Barmack and Yakhnitsa, 2008).…”

“…The cell-to-cell variability of movement-related discharges in GCs was also observed for various eye and head movements (Miles et al, 1980) and forelimb manipulations (van Kan et al, 1993) in the monkey, as well as during cat locomotion (Edgley and Lidierth, 1987). This was vexingly not the case for electrical and somatosensory stimuli of vibrissal pads and limbs in rats (Vos et al, 1999b;Holtzman et al, 2006), in which the evoked GC responses were more stereotypical.…”

“…They were often followed by a negative after-wave (NAW) and were difficult to keep isolated for longer times. Based on previous similar descriptions from awake monkey recordings (Kase et al, 1980;Miles et al 1980;Ohtsuka and Noda, 1992;van Kan et al 1993), we assigned these action potentials to be emanating from MF terminals. The ISI histograms computed for these units were, however, highly diverse and unlike for GCs, typical histograms exemplifying the putative MFs could not be provided.…”