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 degrees/s pulses of head velocity. VOR adaptation was studied by having the monkeys wear x2 or x0.25 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.

FIG. 1

Views of the floccular-complex of the monkey cerebellum from the postero-lateral side (A) and the ventral side (B). Numbered folia are part of the floccular complex. Folia 1–4 comprise the flocculus, while folia 5–10 comprise the ventral paraflocculus. PL, petrosal lobule; DPF, dorsal paraflocculus; PLF, postero-lateral fissure; VII, facial nerve; VIII, vestibulo-cochlear nerve.

FIG. 2

Schematic drawing summarizing all the lesions of the floccular complex in our 5 monkeys and in the 2 monkeys from Lisberger et al. (1984). Each square represents one folium on one side of the brain in one monkey. Black, gray, and white filling indicate folia that were completely absent, partially present, or intact. Folia 1– 4 comprise the flocculus, and folia 5–9 are part of the ventral paraflocculus. The lesions are grouped according to the extent of the lesions. Two lesions of the flocculus are shown in the group at the left of the figure (Group I), 2 unilateral lesions of ventral paraflocculus are shown in the middle group (Group II), and 3 large lesions including both flocculus and ventral paraflocculus are shown in the group at the right of the figure (Group III).

FIG. 3

Coronal sections of the right and left floccular-complex in a control monkey (A), a monkey with a bilateral lesion of the flocculus (B), and a monkey with a unilateral lesion of the ventral paraflocculus (C). From top to bottom the sections proceed from rostral to caudal, and each row of sections was taken from the same rostral-caudal level in different monkeys. The numbers alongside each section indicate the folia of the flocculus and ventral paraflocculus that are present. VIII, vestibular nerve; PL, the petrosal lobule; PLF, postero-lateral fissure.

FIG. 4

Absence of deficits in smooth pursuit eye movements or motor learning in the vestibuloocular reflex (VOR) of 2 monkeys with bilateral lesions of the flocculus. The top and bottom panels show results for monkeys Gu and Ca, respectively. A and B: averages of smooth eye velocity as a function of time for target motion to the right and left at 10, 20, and 30°/s. Solid and dashed traces show prelesion and postlesion data, respectively. Upward deflections show rightward eye velocity. Numbers next to the traces indicate the ramp target velocity for step-ramp target motions. C and D: gain of the VOR in the dark is plotted as a function of the day of the recording. “×2” and “×0.25” indicate results for spectacles that magnified or miniaturized vision. Open symbols and solid traces show the time course of motor learning before the lesion. Filled symbols and dashed traces show the time course of motor learning after the lesion. Note that the y-axis plots the change in the gain of the VOR relative to the control value before the spectacles were placed on the monkey for each adaptation.

FIG. 5

Small deficits in smooth pursuit eye movements and motor learning in the VOR of 2 monkeys with unilateral lesions of the ventral paraflocculus. A–D: averages of smooth eye velocity as a function of time for horizontal (A and C) and vertical (B and D) target motion at 10, 20, and 30°/s. The 2 monkeys are shown as the left and right pairs of traces. Fine traces with SDs show prelesion data, and bold traces show postlesion data. Upward deflections show rightward eye velocity. Numbers next to the traces in A indicate the ramp target speed for step-ramp target motions. E–G: bar graphs quantifying parameters of smooth pursuit by showing the mean and SD of latency (E), initial eye acceleration (F), and steady-state eye velocity (G) for pursuit of step-ramp target motion at 30°/s. The 2 graphs in each panel show data for the 2 monkeys. Open and filled bars show data from before and after the lesion. Asterisks indicate statistically significant (P < 0.05) effects of the lesion. H and I: gain of the VOR in the dark is plotted as a function of the day of the recording. “×2” and “×0.25” indicate results for spectacles that magnified or miniaturized vision. Open symbols and solid traces show the time course of motor learning before the lesion. Filled symbols and dashed traces show the time course of motor learning after the lesion. Note that the y-axis plots the change in the gain of the VOR relative to the control value before the spectacles were placed on the monkey for each adaptation.

FIG. 6

Coronal sections of the right and left floccular-complex in a control monkey (A) and 2 monkeys with large bilateral lesions of the flocculus and ventral paraflocculus (B). Monkey Da (middle column) is one of our monkeys, and monkey Cr (right column) is a monkey from Lisberger et al. (1984). From top to bottom the sections proceed from rostral to caudal; each row of sections was taken from the same rostral-caudal level. The numbers alongside each section indicate the folia of the flocculus and ventral paraflocculus that are present. VIII, vestibular nerve; PL, the petrosal lobule; PLF, postero-lateral fissure.

FIG. 7

Large deficits in smooth pursuit eye movements and motor learning in the VOR in a monkey with large bilateral lesions of the flocculus and ventral paraflocculus. A and B: averages of smooth eye velocity as a function of time for horizontal (A) and vertical (B) target motion at 10 and 30°/s. Fine traces with SDs show prelesion data, and bold traces show postlesion data. Upward deflections show rightward eye velocity. Numbers next to the traces indicate the ramp target speed for step-ramp target motions. C: bar graphs quantifying parameters of smooth pursuit by showing the mean and SD of latency (top), initial eye acceleration (middle), and steady-state eye velocity (bottom) for pursuit of step-ramp target motion at 30°/s. Open and filled bars show data from before and after the lesion. Asterisks indicate statistically significant (P < 0.05) effects of the lesion. D: gain of the VOR in the dark is plotted as a function of the day of the recording. “×2” and “×0.25” indicate results for spectacles that magnified or miniaturized vision. Open symbols and solid traces show the time course of motor learning before the lesion. Filled symbols and dashed traces show the time course of motor learning after the lesion. Note that the y-axis plots the change in the gain of the VOR relative to the control value before the spectacles were placed on the monkey for each adaptation.