Mechanisms underlying vestibulo-cerebellar motor learning in mice depend on movement direction.

Kai Voges,Chris I De Zeeuw,Martijn Schonewille,Bin Wu,Laura Post

doi:10.1113/jp274346

Kai Voges, Chris I De Zeeuw + Show 3 more

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https://doi.org/10.1113/jp274346

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Abstract

Key points Directionality, inherent to movements, has behavioural and neuronal correlates.Direction of vestibular stimulation determines motor learning efficiency.Vestibulo‐ocular reflex gain–increase correlates with Purkinje cell simple spike potentiation.The locus of neural correlates for vestibulo‐ocular reflex adaptation is paradigm specific. Compensatory eye movements elicited by head rotation, also known as vestibulo‐ocular reflex (VOR), can be adapted with the use of visual feedback. The cerebellum is essential for this type of movement adaptation, although its neuronal correlates remain to be clarified. In the present study, we show that the direction of vestibular input determines the magnitude of eye movement adaptation induced by mismatched visual input in mice, with larger changes during contraversive head rotation. Moreover, the location of the neural correlate of this changed behaviour depends on the type of paradigm. Gain–increase paradigms induce increased simple spike (SS) activity in ipsilateral cerebellar Purkinje cells (PC), which is in line with eye movements triggered by optogenetic PC activation. By contrast, gain–decrease paradigms do not induce changes in SS activity, indicating that the murine vestibulo‐cerebellar cortical circuitry is optimally designed to enhance ipsiversive eye movements.

Highlights

As a result of the structure and connections of their receptors, afferents from the vestibular and visual system carry inherently direction-selective information (Ezure & Sasaki, 1978; Lopez-Barneo et al 1982)
For the solely vestibularly driven vestibulo-ocular reflex (VOR) (Fig. 1B and C), gains were not significantly different for the two directions (n = 31, P = 0.10, t = 1.64) but, in line with the visual vestibulo-ocular reflex (VVOR) data described above, VOR delays were shorter for the eye movements in the t–n direction (P < 0.001, t = 6.20)
To test the hypothesis that cerebellar learning depends on movement direction, we investigated to what extent compensatory eye movements and VOR gain–increase and gain–decrease adaptation are direction-specific

Summary

Introduction

As a result of the structure and connections of their receptors, afferents from the vestibular and visual system carry inherently direction-selective information (Ezure & Sasaki, 1978; Lopez-Barneo et al 1982) In principle, this type of information may be relevant for cerebellar motor learning, such as goal-directed adaptation of reaching tasks of the limbs, smooth pursuit eye movements or compensatory eye movements (CEMs) (Robinson, 1976; Distler & Hoffmann, 2003; Smith & Shadmehr, 2004; Tseng et al 2007; Cahill & Nathans, 2008; Medina & Lisberger, 2008). Sensory and motor information required for motor learning is conveyed to the cerebellar cortex through two main afferent systems (Gao et al 2012).

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