The ability to orient and navigate through the terrestrial environment represents a computational challenge common to all vertebrates. It arises because motion sensors in the inner ear, the otolith organs, and the semicircular canals transduce self-motion in an egocentric reference frame. As a result, vestibular afferent information reaching the brain is inappropriate for coding our own motion and orientation relative to the outside world. Here we show that cerebellar cortical neuron activity in vermal lobules 9 and 10 reflects the critical computations of transforming head-centered vestibular afferent information into earth-referenced self-motion and spatial orientation signals. Unlike vestibular and deep cerebellar nuclei neurons, where a mixture of responses was observed, Purkinje cells represent a homogeneous population that encodes inertial motion. They carry the earth-horizontal component of a spatially transformed and temporally integrated rotation signal from the semicircular canals, which is critical for computing head attitude, thus isolating inertial linear accelerations during navigation.

1. Upper eyelid position and velocity, and the electromyographic (EMG) activity of the orbicularis oculi muscle, were recorded bilaterally in alert cats during spontaneous, reflexively evoked, and conditioned eyelid movements. 2. Spontaneous blinks appeared randomly (0.2-0.5 per min) and consisted of a fast, large downward lid movement followed by a slower up phase. Blinks of smaller amplitude and slower velocity were also observed mainly accompanying behavioral movements, such as during peering and grimacing. 3. Eyelid response to air puffs applied to the cornea and tarsal lid skin consisted of a short-latency (9-16 ms), fast (up to 2,000 degrees/s) downward movement that lasted for 25-30 ms, followed by late, small downward sags that were sometimes still evident after stimulus offset. Blinks outlasted the duration of the stimulus by approximately 150 ms. Blinks elicited by flashes of light or tones showed longer latency (47.3 +/- 6.3 and 53.7 +/- 8.0 ms, mean +/- SD; respectively), smaller amplitude, and a quicker habituation than air-puff-evoked lid responses. 4. For the down phase of the blink, the peak velocity, but not its duration, increased linearly with blink amplitude. Because the rise time of the down phase remained constant, changes in blink amplitude seemed to be the result of increased blink velocity. The down phase of a typical 10 degrees blink was 10 times faster than the up phase of the same blink or than upward and downward lid saccades of the same amplitude. The peak velocity and duration of the up phases of reflex blinks and upward and downward lid saccades increased linearly with lid movement amplitude. 5. The initial down phase of air-puff-evoked blinks decreased in latency, increased in amplitude and peak velocity, and maintained the same rise time for increasing puff pressure. None of these parameters was dependent on puff duration. The duration of the blink also increased linearly with air puff duration. 6. The amplitude of air-puff-evoked blinks was inversely related to lid position, decreasing with further lid positions in the closing direction. In contrast, neither peak nor integrated EMG activity of the orbicularis oculi muscle was affected by lid position, being only a function of stimulus parameters and of the animal's level of alertness. 7. Air puffs > 20 ms and > 1 kg/cm2 evoked two successive bursts (R(ap) 1 and R(ap) 2) in the EMG activity of the orbicularis oculi muscle. Shorter and/or weaker stimuli evoked only the R(ap) 1 response.(ABSTRACT TRUNCATED AT 400 WORDS)

Spatial orientation depends critically on the brain's ability to segregate linear acceleration signals arising from otolith afferents into estimates of self-motion and orientation relative to gravity. In the absence of visual information, this ability is known to deteriorate at low frequencies. The cerebellar nodulus/uvula (NU) has been shown to participate in this computation, although its exact role remains unclear. Here, we show that NU simple spike (SS) responses also exhibit a frequency dependent selectivity to self-motion (translation) and spatial orientation (tilt). At 0.5 Hz, Purkinje cells encode three-dimensional translation and only weakly modulate during pitch and roll tilt (0.4 Ϯ 0.05 spikes/s/°/s). But this ability to selectively signal translation over tilt is compromised at lower frequencies, such that at 0.05 Hz tilt response gains average 2.0 Ϯ 0.3 spikes/s/°/s. We show that such frequency-dependent properties are attributable to an incomplete cancellation of otolith-driven SS responses during tilt by a canal-driven signal coding angular position with a sensitivity of 3.9 Ϯ 0.3 spikes/s/°. This incomplete cancellation is brought about because otolith-driven SS responses are also partially integrated, thus encoding combinations of linear velocity and acceleration. These results are consistent with the notion that NU SS modulation represents an internal neural representation of similar frequency dependencies seen in behavior.

The striatum of the basal ganglia is considered a key structure in the learning circuitry of the brain. To analyze neural signals that underlie striatal plasticity, we recorded from an identifiable class of striatal interneurons as macaque monkeys underwent training in a range of conditioning and non-associative learning paradigms, and recorded eyeblink electromyographs as the measure of behavioral response. We found that the responses of these striatal interneurons were modifiable under all training conditions and that their population responses were tightly correlated with the probability that a given stimulus would evoke a behavioral response. Such a network signal, proportional to current response probability, could be crucial to the learning and decision functions of the basal ganglia.

The vestibulo-ocular reflex (VOR) comprises an outstanding system to perform studies that probe possible cerebellar roles in motor learning. Novel VOR gains can be induced (learned) by the wearing of minifying or magnifying lenses, and learning requires the presence of the cerebellum. Previously, it was shown that Purkinje cells change their head velocity sensitivities with learning and that this change was thought to be inappropriate to be causal for the changed behavior. We now demonstrate that Purkinje cells also change their eye position, eye velocity, and head velocity sensitivities after learning. These combined changes at the Purkinje cell level contribute to a net modulation that is appropriate to support the new VOR gains. Importantly, the changes in the eye position parameter, reported for the first time, suggest the involvement of the neuronal integrator pathways in VOR learning. We provide evidence that all of these changes are necessary for VOR behavior and can explain learning deficits after cerebellar removal.