Research reportThe brain during free movement – What can we learn from the animal model
Introduction
Unlike humans, animals will not voluntarily sit still during the execution of scientific experiments. However, since they are also not able to respond to behavioral probing through speaking and only in a few cases can answer by a button press or a directed eye movement, animals actually need to move their bodies in order to convey information about the outcome of cognitive processes. Therefore, when studying the role of the brain in cognitive functioning, animal researchers have to embrace the movements of their experimental subjects rather than suppress them. Scientists indeed have come up with many diverse techniques to make this possible.
In comparison, studying the human brain, there seems less need to provide participants with the freedom to move. Language gives us the possibility to convey complex information without actually needing to enact it. Even looking at locomotion as the epitome of free movement, there are many possibilities to test single aspects of this while restricting the actual freedom to move to a minimum. Freely moving through space is an intentional action based on spatial navigation, active sensing and motor planning. Using elaborate setups including virtual reality, treadmills, and focusing on planning very small movements these aspects can be studied in humans without allowing actual locomotion. However, this is only possible to a limited extent, especially concerning the complex interplay between these processes. Additionally, recent behavioral research has made very clear that the movement of the whole body can also affect a surprising number of cognitive functions, which on first sight seem to be independent of large body movements. These include memory, attention, and sensory integration (Schmidt-Kassow et al., 2013, Schmidt-Kassow et al., 2014, Kirsch, et al., 2017, Schaefer et al., 2010, McMorris and Graydon, 2000, Smith et al., 2010). Animal studies have shown similar effects in freely moving animals, whilst concurrently starting to uncover how brain activity is affected by free movements (Niell and Stryker, 2010, Polack et al., 2013, Saleem et al., 2013). Since neurophysiological measurements in humans during free walking are exceedingly rare, this review focuses on locomotion in animals and omits other research on free movements such as from the arm or hand. Human research might profit most readily from these animal studies during locomotion.
Despite the fact that portable recording systems were developed in animals out of sheer necessity to allow the animal to convey information through body movements, findings from ongoing animal research can be most useful for human research in this field. The benefit can be at least twofold: 1) the technical advancements enabling researchers to study the animal brain during large movements might inspire technologies to record neural activity in the moving human brain, and 2) the ongoing animal research might help to formulate hypotheses or shape promising experimental questions based on results from the animal model. It is our belief that the full potential of these benefits has not yet been met.
This review is divided into two main parts: first, we address the methodological developments and challenges in research on freely moving animals. Second, we discuss experimental questions in animal research that specifically address the interaction between brain activity and free movements with a focus on locomotion in mammals. We discuss how important the role of free locomotion is for understanding spatial navigation, active sensing, and complex motor planning. Additionally, we propose the idea of regarding movement as the expression of a behavioral state. In this view, free locomotion is the most active state of a wide range of behavioral states, including sleeping and being quietly awake. We suggest thinking about freely walking as a specific behavioral state since it calls for very specific processing of external stimuli and generating motor output. This view helps to understand the general influence of movement on brain function.
Section snippets
Recording brain activity during movement
Broadly speaking, the techniques for recording neural activity from the brain fall into two categories. There are those that directly measure electrical activity from neurons using e.g. microelectrodes, electroencephalography (EEG) or electrocorticography (ECoG), and those that measure neuronal activity indirectly by imaging the metabolic activity of neurons, such as functional magnetic resonance imaging (fMRI), positron emission tomography (PET), and calcium imaging. These sets of methods have
Movement as an intentional action
Moving animals execute motor behavior; their muscles contract and relax in an organized fashion, as a result of which the animal moves. This can happen stereotypically, such as in reflex or in cases where a sensory input leads to a highly predefined motor output due to overtrained response behavior (e.g. button presses or saccades to a target). Free movement, however, is much more than this. Freely moving animals not only passively react to incoming information from the surround but also act on
Conclusion
In conclusion, free movement can affect a surprising number of cognitive functions, which on first sight seem to be independent of large body movements. Besides the obvious necessity of motion for investigating motor activity, these other cognitive functions need to be considered also in human experimentation. We have shown that animal research that has been done in the fields of spatial navigation, motor planning and active sensing can directly help to understand these cognitive domains in
Acknowledgements
We want to thank Michael Berger for valuable discussions, Roland Pfister for helpful comments on the manuscript, and all the authors of the original figures for kindly sharing their work. Händel, B.F., is supported by an ERC starting grant (677819 — BBRhythms).
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