Motor Coding in Floccular Climbing Fibers

2006 ◽  
Vol 95 (4) ◽  
pp. 2342-2351 ◽  
Author(s):  
Beerend Winkelman ◽  
Maarten Frens

The climbing fibers (CFs) that project from the dorsal cap of the inferior olive (IO) to the flocculus of the cerebellar cortex have been reported to be purely sensory, encoding “retinal slip.” However, a clear oculomotor projection from the nucleus prepositus hypoglossi (NPH) to the IO has been shown. We therefore studied the sensorimotor information that is present in the CF signal. We presented rabbits with visual motion noise stimuli to break up the tight relation between instantaneous retinal slip and eye movement. Strikingly, the information about the motor behavior in the CF signal more than doubled that of the sensory component and was time-locked more tightly. The contribution of oculomotor signals was independently confirmed by analysis of spontaneous eye movements in the absence of visual input. The motor component of the CF code is essential to distinguish unexpected slip from self-generated slip, which is a prerequisite for proper oculomotor learning.

1980 ◽  
Vol 43 (1) ◽  
pp. 182-206 ◽  
Author(s):  
N. H. Barmack ◽  
J. I. Simpson

1. Discrete, unilateral, electrolytic lesions of the dorsal cap of the inferior olive were made in rabbits in an attempt to assess the effect on eye movements of removal of a visual climbing fiber input to the fluocculus. The position of the lesioning electrode within the dorsal cap was adjusted on the basis of the field potential evoked by flash stimulation of the contralateral eye. 2. Electrophysiological and anatomical evidence confirmed that the microlesions of the dorsal cap destroyed 10-80% of olivary cells, but cause only slight damage to the olivocerebellar pathway originating from the contralateral dorsal cap. 3. The immediate effect of the microlesions was a spontaneous, conjugate drift of the eyes to the side contralateral to the lesion. The effects of the microlesions on eye movements were further examined using reflexes evoked by vestibular and optokinetic stimulation. 4. Postoperatively, the vestibuloocular reflex (VOR) gain was not modified, but there was a marked VOR velocity bias to the contralateral side. This velocity bias was most pronounced at low stimulus frequencies (0.02-0.05 Hz, +/- 10 degrees) and was minimal at stimulus frequencies above 0.5 Hz. 5. Monocular, sinusoidal optokinetic stimulation with a large contrast-rich visual target evokes, in normal rabbits, a conjugate asymmetric following response with a higher eye velocity for target movement from posterior to anterior. Following damage to the dorsal cap, the asymmetry of this optokinetic reflex was reversed when the target was presented to the eye contralateral to the lesion. With monocular, constant-velocity optokinetic stimulation delivered to the contralateral eye, the optokinetic gain for movement in the posterior to anterior direction was decreased. 6. These data suggest that visual climbing fibers are part of a feedback loop that reduces retinal slip of low velocity. The relatively low discharge rate of climbing fibers would seem appropriate to ecode continuously retinal slip of low velocity and to influence low-velocity eye movements.


1974 ◽  
Vol 52 (6) ◽  
pp. 1212-1217 ◽  
Author(s):  
J. Courville ◽  
F. Faraco-Cantin ◽  
N. Diakiw

The olivo–cerebellar projection has been demonstrated by injections of small volumes of tritiated l-leucine in the inferior olive. A strictly contralateral projection to the cerebellar cortex has been found. Labelling of terminal fibers in the molecular layer is restricted to the paravermian and lateral regions of cortex after an injection of the central region of the olive. The distribution presents a very striking feature: the label is distributed along sagittal bands about 0.4 mm wide interrupted by empty spaces of the same width. It is suggested that an extra-olivary source provides the climbing fibers distributed in these spaces.


1981 ◽  
Vol 24 (1) ◽  
pp. 103-108 ◽  
Author(s):  
E. Chung Hwang ◽  
A. Plaitakis ◽  
I. Magnussen ◽  
M.H. Van Woert

2003 ◽  
Vol 90 (4) ◽  
pp. 2349-2357 ◽  
Author(s):  
Daniel A. Nicholson ◽  
John H. Freeman

The development of synaptic interconnections between the cerebellum and inferior olive, the sole source of climbing fibers, could contribute to the ontogeny of certain forms of motor learning (e.g., eyeblink conditioning). Purkinje cell complex spikes are produced exclusively by climbing fibers and exhibit short- and long-latency activity in response to somatosensory stimulation. Previous studies have demonstrated that evoked short- and long-latency complex spikes generally occur on separate trials and that this response segregation is regulated by inhibitory feedback to the inferior olive. The present experiment tested the hypothesis that complex spikes evoked by periorbital stimulation are regulated by inhibitory feedback from the cerebellum and that this feedback develops between postnatal days (PND) 17 and 24. Recordings from individual Purkinje cell complex spikes in urethan-anesthetized rats indicated that the segregation of short- and long-latency evoked complex spike activity emerges between PND17 and PND24. In addition, infusion of picrotoxin, a GABAA-receptor antagonist, into the inferior olive abolished the response pattern segregation in PND24 rats, producing evoked complex spike response patterns similar to those characteristic of younger rats. These data support the view that cerebellar feedback to the inferior olive, which is exclusively inhibitory, undergoes substantial changes in the same developmental time window in which certain forms of motor learning emerge.


1993 ◽  
Vol 70 (1) ◽  
pp. 117-127 ◽  
Author(s):  
G. D. Kaufman ◽  
J. H. Anderson ◽  
A. J. Beitz

1. The effects of acute and chronic labyrinthectomies on Fos-defined neuronal activity induced by rotation were determined with the use of quantitative image analysis procedures. Unilateral sodium arsanilate labyrinthectomies (UL) were performed either 24 h (acute) or 2 wk (chronic) before exposure to a 90 min, 2-G centripetal acceleration along the interaural axis that stimulated the intact otolith organs. The results obtained from both acute and chronic UL animals subjected to centripetal acceleration were compared with data obtained from nonrotated UL animals and fully intact, normal animals exposed to centripetal acceleration. Such comparisons allowed the definition of functional projections from the otolith organs of one labyrinth to vestibular related and inferior olivary brain stem nuclei in the rat. 2. The effect of the labyrinthectomy on nonrotated animals was first assessed. After acute UL, asymmetric Fos expression was present in the medial and inferior vestibular nuclei, the prepositus hypoglossi (bilaterally), the ipsilateral (with respect to the side of UL) dorsolateral periaqueductal gray, and the contralateral inferior olivary beta subnucleus, as previously described (Kaufman et al., 1992b). Except for minimal labeling in the contralateral prepositus hypoglossi and the dorsolateral periaqueductal gray, the Fos labeling that was present in the brain stem of acute UL animals was absent in chronic UL animals. Thus Fos neuronal activity appears to define a pattern of brain stem activation associated with the initial events that underlie vestibular compensation. 3. In acute UL rats, which were rotated, the contralateral beta subnucleus of the inferior olive had greater labeling (compared with nonrotated UL animals) when the lesion was away from the axis of rotation. In contrast, the ipsilateral beta subnucleus labeled when the lesion was towards the axis of rotation. Fos expression was observed bilaterally in the prepositus hypoglossi when the lesioned side was oriented toward the axis of rotation but was observed only in the contralateral prepositus nucleus when the lesioned side was oriented away from the axis of rotation. Finally, the dorsomedial cell column of the inferior olive (DMCC) was heavily labeled when the lesioned side was oriented towards the axis of rotation but was unlabeled when the lesioned side was oriented away from the axis of rotation. In acute UL nonrotated animals the DMCC was only lightly labeled. All other brain stem nuclear labeling was similar between the acute UL rotated and nonrotated animals.(ABSTRACT TRUNCATED AT 400 WORDS)


1982 ◽  
Vol 48 (4) ◽  
pp. 952-967 ◽  
Author(s):  
J. Wallman ◽  
J. Velez ◽  
B. Weinstein ◽  
A. E. Green

1. This study demonstrates plasticity of the vestibuloocular reflex (VOR) in chickens and compares it to that of other species and to that of newly hatched chicks. Adaptive changes in the VOR were induced by subjecting the animals to combinations of visual and vestibular stimuli that simulated the effect of the VOR being either too low in gain or reversed in phase. 2. The VOR of chickens resembles that of mammals, but the curve of phase lead versus frequency seems shifted toward higher frequencies. The VOR of newly hatched chicks has extremely low gain (less than 0.1). 3. In both the older and newly hatched animals, the VOR gain increased substantially after 2 h in an environment in which the imposed en bloc rotations produced increased retinal image slip in the normal directions. Similarly, 2 h of reversed retinal image slip produced decreased VOR gain and, in some cases, reversal fo the phase of the VOR. The gain changes were largest at the "training" frequency. The phase changes were in the direction of increased phase lead. Changes in the gains of the optokinetic responses and of the combination of VOR and optokinetic responses were also seen, especially in the newly hatched animals. 4. The newly hatched birds showed the largest VOR changes in the increased-gain situation, whereas the older birds showed the largest changes in the reversed-phase situation, as assessed by the changes in the average retinal slip velocity experienced. These results may well not be a consequence of differences in age, per se, but of differences in average retinal slip experienced in the two experimental situations at the start of the trial because of the lower VOR gain of the newly hatched animals. There seems to be no dramatic difference in VOR plasticity between newly hatched and older birds. 5. Our results with reversed visual motion are substantially different from those obtained in similar studies on rabbits, suggesting that these two species use different error signals to control the adaptive adjustment of the VOR.


2000 ◽  
Vol 84 (5) ◽  
pp. 2552-2563 ◽  
Author(s):  
M. P. Arts ◽  
C. I. De Zeeuw ◽  
J. Lips ◽  
E. Rosbak ◽  
J. I. Simpson

The caudal dorsal cap (dc) of the inferior olive is involved in the control of horizontal compensatory eye movements. It provides those climbing fibers to the vestibulocerebellum that modulate optimally to optokinetic stimulation about the vertical axis. This modulation is mediated at least in part via an excitatory input to the caudal dc from the pretectal nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic system. In addition, the caudal dc receives a substantial GABAergic input from the nucleus prepositus hypoglossi (NPH). To investigate the possible contribution of this bilateral inhibitory projection to the visual responsiveness of caudal dc neurons, we recorded the climbing fiber activity (i.e., complex spikes) of vertical axis Purkinje cells in the flocculus of anesthetized rabbits before and after ablative lesions of the NPH. When the NPH ipsilateral to the recorded flocculus was lesioned, the spontaneous complex spike firing frequency did not change significantly; but when both NPHs were lesioned, the spontaneous complex spike firing frequency increased significantly. When only the contralateral NPH was lesioned, the spontaneous complex spike firing frequency decreased significantly. Neither unilateral nor bilateral lesions had a significant influence on the depth of complex spike modulation during constant velocity optokinetic stimulation or on the transient continuation of complex spike modulation that occurred when the constant velocity optokinetic stimulation stopped. The effects of the lesions on the spontaneous complex spike firing frequency could not be explained when only the projections from the NPH to the inferior olive were considered. Therefore we investigated at the electron microscopic level the nature of the commissural connection between the two NPHs. The terminals of this projection were found to be predominantly GABAergic and to terminate in part on GABAergic neurons. When this inhibitory commissural connection is taken into consideration, then the effects of NPH lesions on the spontaneous firing frequency of floccular complex spikes are qualitatively explicable in terms of relative weighting of the commissural and caudal dc projections of the NPH. In summary, we conclude that in the anesthetized rabbit the inhibitory projection of the NPH to the caudal dc influences the spontaneous firing frequency of floccular complex spikes but not their modulation by optokinetic stimulation.


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