Contribution of somatosensory input to mechanisms of movement suppression during action observation

Lead Research Organisation: University College London
Department Name: Institute of Neurology

Abstract

Execution of everyday movements as for example grasping of an object appears and feels effortless but requires a sophisticated mechanical machinery of muscles and joints and a complex control system including spinal cord and brain circuits. There is accumulating evidence that large part of this control system is active during movement observation. More than twenty years ago Prof Rizzolatti and colleagues discovered single neurons in area F5 of macaque monkeys brain responding not only to monkey grasping but also to observation of the same grasp performed by human experimenter. These neurons were called "mirror neurons". Our group made a major contribution to the field of mirror neurons by discovering that in area F5 and in primary motor cortex even neurons directly connected to the spinal motor neurons can be modulated just by observation of an action. This apparent paradox of the motor system being active during action observation without production of any movement challenges our understanding of how movements are generated and prompts research to identify what separate movement execution from action observation.
An obvious candidate is somatosensory system that responds to changes to the surface or internal state of the body. Somatosensory input is clearly very different between observation of a grasp when hand is at rest and grasp execution when hand is moving and touching an object. This difference might be an important contributing factor to why movements do not occur during action observation despite mirror neuronal activity present in motor areas. A dramatic examples of how powerful the somatosensory input is for perception is the "rubber hand" illusion: light stroking of subject hand combined with observation of synchronous stroking of an artificial hand forces subjects to believe that an artificial rubber hand is their own and that they can control it.
To understand the possible contribution of somatosensory input to the mechanisms of movement suppression during action observation, we suggest to investigate the somatosensory properties of the mirror neuron system (MNS). This includes responses of single mirror neurons to light touch, hair brushing and passive hand movement. Some neurons in area F5, where mirror neurons where discovered, have been shown to respond to such stimulation but it was not so far tested for mirror neurons. And more specifically we will investigate differences in somatosensory properties of facilitation and suppression mirror neurons discovered in our laboratory.
It is well established that during movement we are less sensitive to the sensory input, eg touch. This reduced sensitivity manifests itself in a smaller neuronal signal in response to electrical stimulation of the nerve in comparison to the response at rest. This phenomenon is called sensory attenuation but it was not tested for mirror neurons. Non-invasive studies aiming at revealing sensory attenuation during action observation are contradictory. Some studies report attenuation while others enhancement. To resolve this controversy it is critical to investigate sensory attenuation on the level of local neuronal signals.
In classical studies of the MNS, subjects just passively observe the actors' movements. In real life, it is quite often an active observation. While we execute an action we simultaneously observe a similar action, e.g. in a shared motor task such as two surgeons working together. Here action observation happens in the presence of somatosensory input, which resembles somatosensory input of an actor. What happens to the MNS simultaneously driven by action execution and action observation? To answer this question we will combine invasive neurophysiological investigation of non-human primates with non-invasive transcranial magnetic stimulation (TMS) studies of human volunteers.

Technical Summary

It is now well established that much of the cortical motor network involved in movement production is active during action observation. We showed that even corticospinal output neurons, projecting from the motor cortex to the spinal cord, can be modulated just by observation of an action, without any sign of movement in the observer. How can these outputs be active without movement? This challenges our understanding of how movements are generated and prompts research to identify neuronal signals that separate movement execution from action observation.
An obvious candidate for such a signal, surprisingly neglected in research so far, is somatosensory input which is clearly very different between passive action observation and action execution. Neurons in area F5, where mirror neurons were discovered, have been shown to receive significant somatosensory input. We suggest to investigate the somatosensory properties of the mirror neuron system (MNS). In particular, we are interested whether facilitation and suppression mirror neurons discovered in our lab show different somatosensory properties. We will test responses of mirror neurons to natural tactile and proprioceptive stimulation. In addition, we will investigate whether response evoked in the MNS by electrical nerve stimulation attenuates/gated during action observation.
In classical studies of the MNS, subjects just passively observe the actors' movements. In real life, it is quite often an active observation. While we execute an action we simultaneously observe a similar action, e.g. in a shared motor task. Here action observation happens in the presence of somatosensory input, which resembles somatosensory input of an actor. What happens to the MNS simultaneously driven by action execution and action observation? To answer this question we will combine invasive neurophysiological investigation of non-human primates with non-invasive transcranial magnetic stimulation (TMS) studies of human volunteers.

Planned Impact

The first impact of the research outlined in this proposal is a basic science impact. Mirror neurons attracted significant amount of public attention and many far reaching claims about their role in explaining how "brain works" have been done. Many of those claims cannot be supported by solid experimental evidences addressing basic properties of mirror neurons. Our laboratory attempts to fill this void by investigating input and output properties of mirror neurons and connectivity within the mirror neuron system. Our findings will promote understanding of the mirror neuron system on the level of single neurons and local field potentials. By combining electrophysiological studies in non-human primates and transcranial magnetic stimulation studies in healthy human volunteers using analogous experimental setups we attempt to bridge the gap between animal and human studies of the mirror neurons system.

Secondly, by communicating our findings to as large an audience as possible, we hope to reach experts in sport science and therapy, motor learning, movement disorders and movement rehabilitation. Movement rehabilitation therapies such as for example after stroke, have already been looking into possibility to use movement observation, ie mirror neuron activity, to improve an outcome. Such attempts might be extended and improved by a better understanding of what the mirror neuron system, which is active during both movement execution and observation, can contribute to rehabilitation. It is potentially more bnefitial to the patients to use a combination of (a) movement therapy, (b) movement observation and (c) attempted or performed movements plus simultaneous observation of movements; with the latter being one of the main aims of the proposed project.

Publications

10 25 50
 
Description Animal experiment: ongoing

Human experiment
In a human experiment, we sought to examine the effect of action observation on motor output in the presence of ongoing motor activity due to the subject's own actions. This is a common real-world situation in which action observation occurs, yet possible similarities or distinctions between this form of observation and passive observation have rarely been studied.
Across all subjects, we did not observe a significant change in motor output between when subjects performed an action alone, or when they performed an action and simultaneously observed an action in front of them.
Exploitation Route Animal experiment: ongoing
Human experiment:
Overall, the results from this experiment were inconclusive, as we did not observe a consistent modulation of motor output during concurrent observation and execution relative to simple execution in either congruent or incongruent conditions. Further work is needed in order to understand the role of the mirror neuron system during simultaneous execution and observation of precise grasping actions. This result highlight that action observation effects on motor output are quite weak and can be masked by other ongoing processes, in this case action execution.
Sectors Education

 
Title HpChambers 
Description New implant design, 
Type Of Material Improvements to research infrastructure 
Year Produced 2019 
Provided To Others? No  
Impact We recently modified modified our existing technique for implants. Specifically, combined several implants into one which reduced number of surgical implantation procedures needed. This is a second step in improvement, on a previous step we redesigned our implant to be manufactured from MRI compatible materials, to allow MRI scans after implantation. 
 
Description Marco Davare 
Organisation Brunel University London
Department Department of Clinical Sciences
Country United Kingdom 
Sector Academic/University 
PI Contribution Human experiment has been conceived in discussions with Dr Marco Davare. Steve Jerjian performed experiments in my lab.
Collaborator Contribution Marco provided equipment to do TMS experiments (TMS machine, TMS coils, EMG amplifiers and computer).
Impact A paper is being prepared based on the results of the carried out experiment
Start Year 2019
 
Description Ethical committee lay mambers visit 
Form Of Engagement Activity Participation in an open day or visit at my research institution
Part Of Official Scheme? No
Geographic Reach Local
Primary Audience Public/other audiences
Results and Impact We organised and a visit to our NHP animal facility by lay members of the main UCL Animal Welfare and Ethical Review Body. During this visit myself and another NHP PI spoke about out research, focusing on our goals and the need of animals for our research programme. We gave short presentations about our work accompanied by a live illustration of a typical training session with NHPs.
We got a very positive feedback from the visitors. "It was a fascinating visit and certainly provides us as lay AWERB members with an more informed opinion on the work and facilities at the Institute."
Year(s) Of Engagement Activity 2018
 
Description MonkeyLab 
Form Of Engagement Activity A press release, press conference or response to a media enquiry/interview
Part Of Official Scheme? No
Geographic Reach National
Primary Audience Media (as a channel to the public)
Results and Impact "The Monkey Lab" is a documentary exploring why monkey research is needed. I participated as one of the interviewed scientists.
Year(s) Of Engagement Activity 2017
URL http://www.bbc.co.uk/programmes/p04z4ycj