Partial Ablations of the Flocculus and Ventral Paraflocculus in Monkeys Cause Linked Deficits in Smooth Pursuit Eye Movements and Adaptive Modification of the VOR

Abstract

The vestibuloocular reflex (VOR) generates compensatory eye movements to stabilize visual images on the retina during head movements. The amplitude of the reflex is calibrated continuously throughout life and undergoes adaptation, also called motor learning, when head movements are persistently associated with image motion. Although the floccular-complex of the cerebellum is necessary for VOR adaptation, it is not known whether this function is localized in its anterior or posterior portions, which comprise the ventral paraflocculus and flocculus, respectively. The present paper reports the effects of partial lesions of the floccular-complex in five macaque monkeys, made either surgically or with stereotaxic injection of 3-nitropropionic acid (3-NP). Before and after the lesions, smooth pursuit eye movements were tested during sinusoidal and step-ramp target motion. Cancellation of the VOR was tested by moving a target exactly with the monkey during sinusoidal head rotation. The control VOR was tested during sinusoidal head rotation in the dark and during 30°/s pulses of head velocity. VOR adaptation was studied by having the monkeys wear ×2 or ×0.25 optics for 4–7 days. In two monkeys, bilateral lesions removed all of the flocculus except for parts of folia 1 and 2 but did not produce any deficits in smooth pursuit, VOR adaptation, or VOR cancellation. We conclude that the flocculus alone probably is not necessary for either pursuit or VOR learning. In two monkeys, unilateral lesions including a large fraction of the ventral paraflocculus produced small deficits in horizontal and vertical smooth pursuit, and mild impairments of VOR adaptation and VOR cancellation. We conclude that the ventral paraflocculus contributes to both behaviors. In one monkey, a bilateral lesion of the flocculus and ventral paraflocculus produced severe deficits smooth pursuit and VOR cancellation, and a complete loss of VOR adaptation. Considering all five cases together, there was a strong correlation between the size of the deficits in VOR learning and pursuit. We found the strongest correlation between the behavior deficits and the size of the lesion of the ventral paraflocculus, a weaker but significant correlation for the full floccular complex, and no correlation with the size of the lesion of the flocculus. We conclude that 1) lesions of the floccular complex cause linked deficits in smooth pursuit and VOR adaptation, and 2) the relevant portions of the structure are primarily in the ventral paraflocculus, although the flocculus may participate.

Visual awareness and the cerebellum: possible role of decorrelation control

“…One was a direct pathway with a gain that accurately matched the head-velocity input to the eye-velocity output at high (>1 Hz) frequencies. Thus, the basic gain of the VOR was not stored in the flocculus itself but in the brainstem (Luebke and Robinson, 1994;McElligott et al, 1998;Rambold et al, 2002). The second component was a leaky integrator with time constant 0.5 s, to be consistent with the observation that after cerebellar inactivation the time constant of postsaccadic drift is longer than that obtained for the plant alone (Carpenter, 1972;Robinson, 1974;Zee et al, 1981;Godaux and Vanderkelen, 1984).…”

“…The brainstem B, intended to represent the medial vestibular nucleus and nucleus prepositus hypoglossi, had two components (details in Appendix). Their characteristics were intended to match those displayed after lesions of the flocculus in primate (Zee et al, 1981;Rambold et al, 2002). One was a direct pathway with a gain that accurately matched the head-velocity input to the eye-velocity output at high (>1 Hz) frequencies.…”

Role of the Dorsolateral Pontine Nucleus in Short-Term Adaptation of the Horizontal Vestibuloocular Reflex

“…Recent lesion studies indicate that the ventral paraflocculus contributes to both smooth pursuit and VOR adaptation (Rambold et al 2002). Therefore it is reasonable that visual mossy fiber input to ventral paraflocculus from DLPN plays a role in smooth pursuit but may not necessarily play a role in adaptation of the VOR.…”

Immunoreactivity for calcium-binding proteins defines subregions of the vestibular nuclear complex of the cat

“…One likely target is oculomotoneurons, since cells retrogradely labeled from tracer injections in the oculomotor and abducens nuclei have been found in the region of high calbindin density at the border of PH and VMN (Graybiel and Hartwieg 1974;Gacek 1977;Langer et al 1986). The cerebellar input suggests the possibility that cells receiving that input are brainstem participants in cerebellar-mediated computational or plastic functions (Rambold et al 2002).…”