Hyper-gravity promotes motor learning in goldfish and humans
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1
Chubu University, Department of Robotic Science and Technology, Japan
Introduction
Microgravity imposes various effects on the human body such as malfunctioning of the cardiovascular system, weakening of muscle strength, reducing calcium from bones, and inducing space motion sickness (Moore, 1996). Further, under micro-gravity, physical movements of astronauts and cosmonauts are slow and somewhat awkward. Motor control systems of our body are continuously calibrated by interacting with gravity on the earth, thus require re-adjustments in the brain motor areas when the gravitational environment is changed. This is not only due to the direct effects of gravity on the mass of the body, but to the effects on sensory systems such as vestibular and proprioceptive systems as well. Although some astronauts have made subjective reports informally, scientific evidence on motor learning under different gravitational environments is missing. In the present study, we address this issue by evaluating learning curves of oculomotor neural integrator adaptation in goldfish and prism adaptation of hand-reaching task in humans under different gravity conditions.
Method and Result in goldfish
We first performed oculomotor neural integrator (NI) adaptation experiments (instability adaptation; Major et al., PNAS, 2004) in goldfish under hyper-gravity (1.5G) and normal gravity conditions. Seven fish (12 - 15cm) were used for the hyper-gravity experiment and the same fish underwent the normal gravity experiment as well. Four fish experienced the hyper-gravity experiment first, while the other 3 fish underwent the normal gravity experiment first. The hyper-gravity environment was created by centrifugation with the apparatus we developed for this experiment. In each condition, the experiment lasted for 2 hours for NI adaptation. Between the two experiments, each fish was given at least 1 week interval in its home water tank. Averaged learning curves of NI time constant (Major et al., PNAS, 2004) over the all fish used under hyper-gravity and normal gravity conditions were compared. As the result, faster learning rate and greater learning amount were found in the mean learning curve of hyper-gravity condition than those in the learning curve of normal gravity condition. Thus, motor learning in goldfish, at least NI adaptation, was promoted under hyper-gravity environment.
Method and Result in humans
Then we conducted motor learning experiments in humans under hyper-gravity (2G) and normal gravity conditions. The motor learning task we employed is prism adaptation of hand-reaching (Martin et al., 1996) which has been a popular motor learning task, and the cerebellum has been identified to crucially be involved (Hanajima, et al., 2015). As in the goldfish experiment, the hyper-gravity environment was created by centrifugation with the GyroLab system. Six healthy male subjects (age 21-42, average 24.7 years old) underwent both hyper-gravity and normal gravity experiments. Each experiment consisted of 20 hand-reaching maneuvers to a visual target on a touch screen at 45 cm in front of the subject without wearing prism goggles, followed by 60 hand-reaching maneuvers to the same target with the prism goggles on. The timing and interval of reaching maneuvers were controlled by the audio instruction recorded before the experiments. The subjects were instructed to close their eyes before they started each reaching maneuver. After each reaching, touched location was immediately marked on the screen, and they were asked to open their eyes to visually confirm where they touched relative to the visual target. Each subject underwent 1G and 2G experiment multiple times (> 4 times for each condition) in a randomized order. Between experiments, subjects were asked to make hand-reaching as many times as possible under normal gravity without wearing prism googles so that they completely readapted to normal visual environment under normal gravity. Averaged learning curves of prism adaptation under hyper-gravity and normal gravity were calculated for each subject, and were compared in each subject. As the result, faster learning rate was found in the mean learning curve of hyper-gravity condition than that in the learning curve of normal gravity condition in all the subjects participated. Therefore, motor learning in humans, at least prism adaptation of hand reaching was promoted under hyper-gravity.
Discussion and hypothesis
Why is motor learning promoted under hyper-gravity in both goldfish and humans? The cerebellum has been implicated to play a crucial role in goldfish NI adaptation and in human hand-reaching prism adaptation. An augmented gravitation input would significantly increase vestibular input to both the goldfish and human cerebellum, in particular, the vestibulocerebellum (VCB). Thus, a working hypothesis for accelerated motor learning under hyper-gravity was envisioned to be an up-regulated Purkinje cell activity enabling more efficient modification of synaptic efficacy. If so then it should be possible to accelerate motor learning by using another stimulus that up-regulates Purkinje cell activity such as that observed in the primate VCB (flocculus) in which Purkinje cells exhibit higher dc firing rates in light than in dark (Hirata and Highstein, 2001). We have also confirmed that similar up-regulation of Purkinje cells in VCB occurs in goldfish (Miki and Hirata, unpublished observation).
Experiment to test the hypothesis
We then tested this experimental paradigm in the goldfish VCB responsible for NI adaptation by inducing motor learning utilizing two types of visual stimuli. Either white spots were displayed as a stimulus on a black background (Darker) or black spots on white background (Brighter). Image contrast of the Darker stimulus was adjusted to evoke an equivalent optokinetic behavior as that induced by the Brighter stimulus so that behavioral error during training would be comparable under the two conditions. The same eight goldfish were used for both Brighter and Darker stimulus experiments. Instability adaptation paradigm was employed. Each NI training experiment lasted for 2 hours as in the hyper-gravity experiment. As a result, a significantly faster learning rate was found with the Brighter than the Darker visual stimulus. This finding supports the hypothesis that Purkinje cell up-regulation alone may produce more efficient changes in synaptic efficacy contributing to the neural basis of motor learning.
Conclusion
Motor learning under hyper-gravity is promoted in humans and goldfish, at least in prism adaptation of hand reaching (human) and oculomotor neural integrator adaptation (goldfish) that we employed in the current study. Similarly, Brighter stimulation promoted motor learning of oculomotor neural integrator adaptation in goldfish. Taken together, it is suggested that cerebellar Purkinje cell up-regulation caused by constant increases of sensory input may accelerate cerebellar synaptic plasticity, and result in promoted motor learning.
References
Moore D, Bie P, Oser E: Biological and Medical Research in Space, Springer, 1996.
Hanajima R, Shadmehr R, Ohminami S, Tsutsumi R, Shirota Y, Shimizu T, Tanaka N, Terao Y, Tsuji S, Ugawa Y, Uchimura M, Inoue M, Kitazawa S: Modulation of error-sensitivity during a prism adaptation task in people with cerebellar degeneration. J Neurophysiol. 114(4):2460-71, 2015 Oct
Major G, Baker R, Aksay E, Mensh B, Seung HS, Tank DW: Plasticity and tuning by visual feedback of the stability of a neural integrator. Proc Natl Acad Sci USA, 101(20):7739-44, 2004, May
Martin TA, Keating JG, Goodkin HP, Bastian AJ, Thach WT: Throwing while looking through prisms: I Focal olivocerebellar lesions impair adaptation. Brain. 119:1183–98, 1996
Hirata Y, Highstein SM: Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol. 85(5):2267-88, 2001 May
Keywords:
Cerebellum,
EYE MOVEMENT,
prism adapation,
synaptic plasiticty,
oculomotor
Conference:
39th ISGP Meeting & ESA Life Sciences Meeting, Noordwijk, Netherlands, 18 Jun - 22 Jun, 2018.
Presentation Type:
Extended abstract
Topic:
Analogues and Countermeasure Research
Citation:
Hirata
Y,
Miura
S,
Takagi
Y,
Kashima
T,
Urase
K and
Miki
S
(2019). Hyper-gravity promotes motor learning in goldfish and humans.
Front. Physiol.
Conference Abstract:
39th ISGP Meeting & ESA Life Sciences Meeting.
doi: 10.3389/conf.fphys.2018.26.00049
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Received:
02 Dec 2018;
Published Online:
16 Jan 2019.
*
Correspondence:
Prof. Yutaka Hirata, Chubu University, Department of Robotic Science and Technology, Kasugai, Japan, yutaka@isc.chubu.ac.jp