Velocity storage mechanism drives a cerebellar clock for predictive eye velocity control

Abstract

predictive motor control is ubiquitously employed in animal kingdom to achieve rapid and precise motor action. in most vertebrates large, moving visual scenes induce an optokinetic response (oKR) control of eye movements to stabilize vision. In goldfish, the OKR was found to be predictive after a prolonged exposure to temporally periodic visual motion. A recent study showed the cerebellum necessary to acquire this predictive OKR (pOKR), but it remained unclear as to whether the cerebellum alone was sufficient. Herein we examined different fish species known to share the basic architecture of cerebellar neuronal circuitry for their ability to acquire pOKR. Carps were shown to acquire pOKR like goldfish while zebrafish and medaka did not, demonstrating the cerebellum alone not to be sufficient. Interestingly, those fish that acquired pOKR were found to exhibit long-lasting optokinetic after nystagmus (OKAN) as opposed to those that didn't. To directly manipulate OKAN vestibularneurectomy was performed in goldfish that severely shortened OKAN, but pOKR was acquired comparable to normal animals. these results suggest that the neuronal circuitry producing oKAn, known as the velocity storage mechanism (VSM), is required to acquire pOKR irrespective of OKAN duration. Taken together, we conclude that pOKR is acquired through recurrent cerebellum-brainstem parallel loops in which the cerebellum adjusts VSM signal flow and, in turn, receives appropriately timed eye velocity information to clock visual world motion.

Homeostatic plasticity of eye movement performance in Xenopus tadpoles following prolonged visual image motion stimulation

“…The flexible interaction between vestibular and visual motion signals in cerebellar circuits has been the focus of numerous experimental studies (e.g., [ 12 ]; see [ 8 ]) largely based on earlier theoretical considerations [ 13 , 14 ]. Key to the outcome of such studies was the importance of the connectivity between the inferior olive and the cerebellum in mediating adaptive plasticity [ 10 , 15 ]. The majority of these studies explored the role of the cerebellum in adapting vestibular motion-evoked eye movements under specific sensory conditions (e.g., visuo-vestibular mismatch; [ 16 ]) or after a loss of head/body motion-related sensory signals (e.g., labyrinthectomy; [ 17 ]).…”

Oculomotor plant and neural dynamics suggest gaze control requires integration on distributed timescales

“…Moreover, models capturing integration on multiple, distributed timescales proposed in previous work on the larval zebrafish hVPNI (Miri, Daie, Arrenberg et al., 2011) have been extended to interpret response diversity among oculomotor integrator neurons in monkeys (Joshua et al., 2013). Having established here that long response timescales are not unique to the primate oculomotor plant, the neural dynamics that compensate for this plant behaviour, and their tuning by the cerebellum, may be further addressed in the larval zebrafish, which is particularly amenable to circuit‐level analysis (Ahrens et al., 2012; Arrenberg & Driever, 2013; Friedrich et al., 2013; Orger et al., 2008; Miki et al., 2020; Aizenberg & Schuman, 2011) and has achieved prominence in the study of visuomotor behaviour (Bianco et al., 2011; Gahtan et al., 2005; Helmbrecht et al., 2018; Okamoto et al., 2008; Portugues & Engert, 2009; Sylvester et al., 2017). We note that leaky integration of velocity signals on distributed timescales in the hVPNI still requires the generation of firing that persists much longer than typical membrane and synaptic time constants.…”

Oculomotor plant and neural dynamics suggest gaze control requires integration on distributed timescales

“…Thus, the implications of these timescales for compensation by motor circuits may be further addressed in a range of model organisms including the larval zebrafish, which is particularly amenable to circuit-level analysis (Ahrens et al 2012; Arrenberg and Driever 2013; Friedrich et al 2013; Orger et al 2008) and has achieved prominence in the study of visuomotor behaviour (Bianco et al 2011; Gahtan et al 2005; Helmbrecht et al 2018; Okamoto et al 2008; Portugues and Engert 2009; Sylvester et al 2017). For example, how the cerebellum contributes to oculomotor integration by tuning brainstem circuits could also be fruitfully addressed using the larval zebrafish model (Miki et al 2020; Aizenberg and Schuman 2011).…”

“…Moreover, models capturing integration on multiple, distributed timescales proposed in previous work on the larval zebrafish hVPNI (Miri et al 2011a) have been extended to interpret response diversity among oculomotor integrator neurons in monkeys (Joshua et al 2013). Having established here that that long response timescales are not unique to the primate oculomotor plant, the neural dynamics that compensate for this plant behaviour, and their tuning by the cerebellum, may be further addressed in the larval zebrafish, which is particularly amenable to circuit-level analysis (Ahrens et al 2012; Arrenberg and Driever 2013; Friedrich et al 2013; Orger et al 2008; Miki et al 2020; Aizenberg and Schuman 2011) and has achieved prominence in the study of visuomotor behaviour (Bianco et al 2011; Gahtan et al 2005; Helmbrecht et al 2018; Okamoto et al 2008; Portugues and Engert 2009; Sylvester et al 2017). We note that leaky integration of velocity signals on distributed timescales in the hVPNI still requires the generation of firing that persists much longer than typical membrane and synaptic time constants.…”