Temporal Firing Patterns of Purkinje Cells in the Cerebellar Ventral Paraflocculus During Ocular Following Responses in Monkeys I. Simple Spikes

Abstract

The simple-spike firing frequency of 30 Purkinje cells (P cells) in the ventral paraflocculus (VPFL) of alert monkeys was studied in relation to vertical slow eye movements, termed ocular following response (OFR), induced by large-field visual motions of different velocities and durations. To quantitatively analyze the relationship between eye movement and firing frequency, an inverse dynamics representation of the eye movement was used for reconstructing the temporal waveform of firing. Coefficients of eye-acceleration, velocity, and position, bias, and time lag between firing and eye movement were estimated by least-square error method. In the regression analyses for each stimulus condition, 86% (146/170) of the well-modulated temporal firing patterns taken from those 30 P cells were reconstructed successfully from eye movement. The model with acceleration, velocity, and position terms, which we used, was shown as the best among several potential models by Cp statistics, consistent with t-test of significance of each term. Reliable coefficients were obtained from 75% (109/146) of the well-reconstructed firing patterns of 28 cells among 30. The estimated coefficients were larger (statistically significant) for slow stimuli than for fast stimuli, suggesting changes in sensitivities under different conditions. However, firing patterns of each cell under several different conditions were frequently well reconstructed by an inverse dynamics representation with a single set of coefficients (13 cells among 21). This indicates that the relationships between P cell firing and OFR are roughly linear in those stimulus ranges. The estimated coefficients for acceleration and velocity suggested that the VPFL P cells properly encode the dynamic components of the motor command during vertical OFR. As for the positional component, however, these P cells are correlated with eye movement in the opposite direction. In the regression analysis without positional component, remarkable differences between observed and reconstructed firing patterns were noted especially in the initial phase of the movements, indicating that the negative positional component was not negligible during OFR. Thus we conclude that, during OFR, the VPFL P cells cannot provide the necessary final motor command, and other brain regions, downstream neural structures, or other types of P cells must provide lacking position-dependent motor commands. This finding about the negative correlation with the position is in the opposite sign with previous studies obtained from the fixation and the smooth pursuit movement. From these comparisons, how the VPFL contributes to a part of the final motor command or how other brain regions complement the VPFL is suggested to be different for early and late phases of the movements.

Large-Field Visual Motion Directly Induces an Involuntary Rapid Manual Following Response

“…These latency differences are, however, much shorter than the time differences between the ocular movement and hand movement reported in previous studies (Turrell et al, 1998;Engel et al, 2000;Soechting et al, 2001), in which efference copy of the ocular motor command is deemed to be used as an arm motor command. Moreover, considering the transmission time from the motor cortex to the arm muscles [11-12 ms for biceps brachii, 14 -15 ms for the brachioradialis, observed by transcranial magnetic stimulation (Abbruzzese et al, 1994)] and the delay from the oculomotor neuron activity to the eye movement [6 -7 ms, which is estimated from and Gomi et al (1998)], the motor command for the MFR would be generated simultaneously with that for the OFR or even earlier.…”

“…The neural control of the OFR involves the middle temporal area (MT) and medial superior temporal area (MST) (Kawano et al, 1994), which encode various types of visual motion signals Wurtz, 1991, 1997;Britten et al, 1993;Movshon and Newsome, 1996). According to several electrophysiological studies on monkeys, the visual motion signals encoded in the MST are sent to the vestibular nuclei via the dorsolateral pontine nucleus (DLPN) (Kawano et al, 1992) and the ventral paraflocculus in the cerebellum Gomi et al, 1998;Takemura et al, 2001). Here, visual motion signals are transformed into the ocular motor commands in terms of eye muscle coordination (kinematics) and the temporal profile (dynamics).…”

“…For example, large-field visual motion induces leg muscle activation with very short latency for stabilizing posture (Nashner and Berthoz, 1978) and induces smooth eye movements [ocular following response (OFR)] for stabilizing retinal images Gellman et al, 1990). Studies of the neural mechanism of the OFR (Kawano et al, 1992(Kawano et al, , 1994Gomi et al, 1998;Takemura et al, 2001) indicate that it is reflexively driven by large-field visual motion and is mediated by a short pathway distinct from those for other, longer-latency types of eye movements. Similar to the oculomotor task, humans often make accurate arm reaching movements during dramatic body movements accompanied by visual motion, for example when a rugby player catches a ball while being pushed by another player.…”

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

“…We tested whether the time course of discharge rate difference was predicted by the discharge modulation associated with smooth pursuit (Fig. 3A, B, green) by the following equation (Gomi et al 1998;Kurkin et al 2003): f (t) = G*smooth pursuit (t-t0) + A…”

From ‘Understanding the Brain by Creating the Brain’ towards manipulative neuroscience

“…R. Soc. B (2008) Kenji Kawano and his colleagues supported the cerebellar feedback-error-learning model with neurophysiological studies in the ventral paraflocculus of the monkey cerebellum during ocular following responses (Shidara et al 1993;Gomi et al 1998;Kobayashi et al 1998;Kawano 1999;Kawato 1999;Takemura et al 2001;Yamamoto et al 2002). The ocular following responses are tracking movements of the eyes evoked by movements in a large visual scene that are thought to be important for visual stabilization of gaze.…”