A differential role for the posterior cerebellum in the adaptive control of convergence eye movements

Abstract

Introduction: The vergence oculomotor system possesses two robust adaptive mechanisms; a fast "dynamic" and a slow "tonic" system that are both vital for single, clear and comfortable binocular vision. The neural substrates underlying these vergence adaptive mechanisms in humans is unclear. Methods: We investigated the role of the posterior cerebellum in convergence adaptation using inhibitory continuous theta-burst repetitive transcranial magnetic stimulation (cTBS) within a double-blind, sham controlled design while eye movements were recorded at 250hz via infrared oculography. Results: In a preliminary experiment we validated our stimulation protocols by reproducing results from previous work on saccadic adaptation during the classic double-step adaptive shortening paradigm. Following this, across a series of three separate experiments we observed a clear dissociation in the effect of cTBS on convergence adaptation. Dynamic adaptation was substantially reduced while tonic adaptation was unaffected. Baseline dynamic fusional vergence response were also unaffected by stimulation. Conclusions: These results indicate a differential role for the posterior cerebellum in the adaptive control of convergence eye movements and provide initial evidence that repetitive transcranial magnetic stimulation is a viable tool to investigate the neurophysiology of vergence control. The results are discussed in the context of the current models of implicit motor adaptation of vergence and their application to clinical populations and technology design in virtual and augmented head mounted display architectures. Significance statement: The cerebellum plays a critical role in the adaptive control of motor systems. Vergence eye movements shift our gaze in depth allowing us to see in 3D and exhibit two distinct adaptive mechanisms that are engaged under a range of conditions including reading, wearing headmounted displays and using a new spectacle prescription. It is unclear what role the cerebellum plays in these adaptive mechanisms. To answer this, we temporarily disrupted the function of the posterior cerebellum using non-invasive brain stimulation and report impairment of only one adaptive mechanism, providing evidence for neural compartmentalization. The results have implications for vergence control models and applications to comfort and experience studies in head-mounted displays and the rehabilitation of clinical populations exhibiting vergence dysfunctions.

Cerebellar rTMS and PAS effectively induce cerebellar plasticity

“…To induce plasticity, we used procedures previously described to be effective in inducing plasticity in the cerebellum. In experiment 1, 1 Hz rTMS 50 , PAS 17 , cTBS 44,51 , and anodal tDCS [64][65][66] was used. 1 Hz rTMS was administered with 90% RMT for 20 min using a Magstim Rapid magnetic stimulator (Magstim Company, Whitland, Dyfed, UK) 50 .…”

“…studies, i.e. 1 Hz rTMS 50 , PAS 17 , cTBS 51 and tDCS 32 . The order of the four plasticity techniques was randomized and they were applied at least one week apart from each other.…”

“…. The intertrial interval was 5 s.CTBS was performed at 50 Hz for 40 s. at 80% AMT using a MagVenture MagOption (MagVenture, Lucernemarken, Denmark)44,51 .…”

Convergence Insufficiency Neuro-Mechanism Adult Population Study: Phoria Adaptation Results

“…45,[83][84][85][86] Yet, human studies using transcranial stimulation support that the posterior portion of the cerebellum is in part responsible for fast fusional vergence adaptation but not for slow fusional vergence. 87 One neurophysiology study of primates supports that the phoria adaptation neural signal is present within the near response cells within the midbrain. 88 Future longitudinal studies are needed to evaluate which neural substrates are correlated to changes with the ability to adapt the phoria after therapeutic intervention.…”

Cerebellar projections to the macaque midbrain tegmentum: Possible near response connections

“…Furthermore, the human cerebellum displays activity related to changes in both vergence angle and lens accommodation (Richter et al, 2000(Richter et al, , 2004Takagi et al, 2003;Lv et al, 2020). In addition, cerebellar lesions produce losses in the ability to adapt aspects of the near response in humans (Milder & Reinecke, 1983;Sander et al, 2009;Leigh & Zee, 2015), and more recently, inactivation of the cerebellum using transcranial magnetic stimulation has been shown to affect the capacity for vergence adaptation (Erkelens et al, 2020).…”