interbrain cortical synchronisation in motor areas encodes aspects of social interaction

Posted comment on ´Interbrain cortical synchronisation encodes multiple aspects of social interactions in monkey pairs` by P. Tseng, S. Rajangam, G. Lehew, M.A. Lebedev and M.A.L: Nicolelis and published in Scientific Reports vol 8 article number 4699 (2018)

SUMMARY

Tseng and colleagues in their article describe interbrain cortical synchronization (ICS) of neural firing representing spatial social interactions in pairs of monkeys observed whilst both subjects participated in a whole body navigation task. The authors began their article by describing the importance to individuals of observing behaviours of others in a group such as learning social rankings, recognising threats and allies and learning new motor skills. Previous research has showed that in primates observation of an action performed by another produced neuronal activity in certain brain areas of the observer eg. frontal and parietal cortices that mirrors that of the primate actually carrying out the action. Those firing neurons have been termed mirror neurons and were defined by Tseng and colleagues as those cortical neurons that respond in the same way when a subject performs or observes an action.

Tseng and colleagues wanted to investigate the neuronal correlates of spatial social interactions in primates and how the social interaction between a monkey pair was affected by whole-body movements of either the dominant or the subordinate animal. In order to overcome the common problem of obtaining concurrent neuronal recordings, Tseng and team used a whole body navigation task with a pair of monkeys, one of whom performed the task and the other observed. Three monkeys (C, K and J – the level of dominance in the group was determined prior to the experiment by the order of priority for food access) were used in the experiments and their brains were implanted with multiple cortical microelectrode arrays. For the experiments the monkeys were paired as C-K and C-J and they performed a whole body navigation task where one monkey (the passenger) was carried in a robotic wheelchair on a randomly computer generated route to a food dispenser giving out grapes while the second monkey (the observer) was seated stationary in a chair in a corner of an approx. 20 square metre room and observed.  Both received a reward at the same time eg. grapes for the passenger who performed the action and juice for the observer to maintain its attention. The monkeys swapped roles for each given task. As the monkeys performed the navigation task, concurrent neuronal connectivity recordings in the motor cortex (M1) and premotor dorsal area (PMd) were carried out. Episodes of synchrony of the neuronal firing (ICS) were said to represent specific aspects of social interactions in the monkeys.

The results of the experiments showed that there was episodes of ICS observed for each test and when all the results of the tests were amalgamated, the ICS observed depended on the wheelchair kinematics (whole body movements:  translational and rotational velocity and spatial location; room coordinates of the wheelchair), the passenger-observer distance and the passenger-food reward distance. Results showed differences with the various monkey pairing and assigned task roles. ICS episodes were observed for approx. 20% of the total session time for monkey pair C-K and 36% for C-J. For example, when monkey C (the more dominant monkey) was passenger and K was observer episodes of high ICS were more frequent when the distance between the monkeys decreased, but there were less frequent ICS when the monkeys swapped roles. Wheelchair velocity produced the same effect. The monkey pair C-J gave the same result pattern. Also higher levels of ICS were more frequent when monkey C, as passenger, was far away from monkey K and became less frequent when C approached J.

Tseng and colleagues also found that the probability of ICS was also influenced by the distance between passenger and grape dispenser (the position of the reward for the passenger). This appeared to be dependent on pairing since with the C-K pairing then the ICS episodes increased when either monkey was passenger and approached the grape dispenser, but with pairing C-J then ICS decreased when either was close to the grape dispenser. There also appeared to be variations in the results if the actual positions of the observer and grape dispenser were also altered. The probability of ICS also appeared to be dependent on wheelchair velocity. There was an increase in value when the wheelchair had a high rotational velocity for monkey C as passenger and monkey K as observer, but no change occurred if K was the passenger. The results of the C-J pairing were the same.

Tseng and colleagues also correlated their results of ICS to particular brain area activity. They found that with the monkey pairing C-K, when C was passenger then M1-to-M1 synchronisation (primary motor cortex-to-primary motor cortex) was the most frequent (approx. 61% of time) with M1-to-PMd (dorsal premotor cortex) synchronisation approx. 52% of the time and PMd-PMd only 43%. The same pattern was observed when K was passenger (53%, 47%, 44%). The authors also observed differences in brain area activity when the ICS was associated with the passenger`s position and velocity. In this case the dependence on neuronal firing rate was quantified using modulation depth. In these experiments Tseng and team found that the passenger had more velocity and acceleration modulated neuronal firing units in both M1 (velocity=  approx. 44% acceleration =  approx.16% ) and PMd (velocity=  approx. 41%  acceleration =   20% ). These values decreased when the monkey became the observer eg.  M1 (velocity=  approx. 1%  acceleration =  approx. 0% ) and PMd (velocity=  approx. 1%  acceleration =   0% ). They also found differences between the monkey pairs with monkey C modulation depth stronger in the PMd area than M1 when paired with K, but weaker when it was paired with monkey J.

The results also showed that there were brain area differences in neural firing when the position of the wheelchair was altered. Activity in both M1 and PMd units was found to be modulated in both passenger and observer brains. More units were modulated in the passenger brain to the observer (56% to 31%) and the presence of episodes of ICS increased spatial modulation strength (67% in presence, 44% in absence). It was also discovered that spatial modulation strength was higher for the more dominant monkeys.  Therefore, Tseng and colleagues showed that there were changes in firing rate associated with task and social rank. For example, it was shown that there was a change in firing rate of PMd units when the passenger was moved to different room locations. Spatial modulation patterns were also affected by the presence or absence of ICS episodes and the monkeys taking part. For example, the neuronal rate of the PMd unit of monkey C increased with decreasing distance between it and monkey K whether C was the observer or passenger. However, when monkey K was passenger then the firing rate of the PMd unit decreased when it approached monkey C, but increased when it approached the grape dispenser. When monkey K was observer then the firing rate of the PMd unit increased when it approached monkey C, but decreased when it approached the grape dispenser. For monkey K, the spatial modulation was stronger during the episodes of ICS observed.

In order to investigate social interaction further, Tseng and colleagues investigated the probability of ICS when the distance between the monkeys was less than 1 metre. This distance was used since the monkeys were said to experience different behaviour when others are within its extrapersonal space. Research from others shows that this is supported by neurochemical studies where mirror neuron modulation also appears to be different when actions occur within this extrapersonal space. In their experiments, Tseng and colleagues found that neuronal rates increased during the ICS episodes in both passenger and observer when this distance was used, but were lower for the more dominant monkey in the pair and higher for the observer compared to the passenger.

Therefore, Tseng and colleagues concluded from their experiments that cortical neurons modulated their firing rate activity in M1 and PMd areas according to whether the monkey was passenger or observer, and also from the experiment`s task wheelchair position and velocity.  Periods of transient synchronised firing were observed and these periods of high ICS were said by the authors to indicate social interaction between the monkeys. As the passenger moved then his M1 and PMd units responded to his change in physical position. The observer had equivalent cortical neuronal populations (mirror neurons) respond to represent the passenger`s movements and a period of synchronisation of firing occurred (ICS) between the passenger`s brain and the observer`s. The ICS periods reflected the social standing of the monkeys and the assigned roles in the task and varied both in probability and magnitude dependent on wheelchair location and speed (velocity and acceleration), distance between the monkeys and distance from the passenger to the reward.

With regards to social standing, Tseng and colleagues concluded that the ICS observed reflected position in the established monkey`s social hierarchy of their experimental monkeys and also assigned roles in the current task. With respect to behaviour, they found that the dominant monkeys roamed freely in their environment, while the more submissive monkeys suppressed their behaviours in that environment to avoid conflict. In their experiments, monkey C was dominant and strong ICS was measured when monkey C was paired with K especially when the two were close together. Social standing was also linked to the results pertaining to the distance between the monkeys. Activity was observed in the PMd area, but could change relating to the monkey`s position within the social hierarchy and therefore, the authors interpreted the activity as representing different approaches eg. ´someone entering my space` would produce a different neural pattern to ´me entering someone else`s space`. The experiment carried out where the distance between passenger and observer was less than 1metre showed more activity in the brain of the less dominant and when the monkey was the observer instead of the more active, passenger.

The authors also concluded that there is a significant amount of activity in the M1 and PMd areas which is modulated between observer and passenger and this observation is consistent with theories of others that mirror neurons are active in premotor and motor cortical areas and represent the observations of actions relating to wheelchair rotation and velocity. The authors observed that the M1 or PMd neurons had different tuning patterns when the monkey was either navigating or observing, but the modulation depth was comparative suggesting to them the existence of mirror neuron activity. The average modulation depth appeared to be higher when the monkey was a passenger rather than an observer and this they concluded could mean that self-motion elicits a stronger representation. Alternatively, the monkey when assigned the role as observer was not as attentive in the experiment and this reflected the experimental set-up which did not demand the observer to have full attention on the task. An attempt to rectify this was by only scoring when the observer monkey`s head was turned in to centre of the room.

With regards to passenger and reward distance, Tseng and colleagues found that neuronal  activity in the M1 and PMd areas was related to it and was modulated as to whether the monkey was passenger or observer. They proposed that social dominance determined food access and levels of aggression and therefore, the neuronal activity observed reflected a social interaction factor. Activity was attributed to dopaminergic activity which led to the suggestion that rewarded actions may explain the phenomenon of learning by observation and therefore, ICS could be a neuronal manifestation of social learning. It could therefore, facilitate the transfer of knowledge from one individual to another.

Therefore, Tseng and colleagues investigation was described as going beyond the ´mirror-neuron framework of observation mirroring action` since it showed that social interaction caused episodic ICS in multiple motor cortical areas. Since social interaction is described as a type of behaviour where actions are amalgamated with observations, the results of Tseng and colleagues were interpreted as indicating that social interaction between pairs of monkeys can be represented by widespread ICS which merges both action and observation as part of a neurophysiological interactive process taking place simultaneously in the motor cortical areas of multiple primate brains within a social group. Therefore, even though the authors identified that an amalgamation of results was necessary and also other behavioural aspects could have an influence on neural effects eg. eye contact, further research on ICS episodes in motor areas was suggested as a way of increasing knowledge about planned movements and execution in social environments. This research they indicated could also be applied to other species including humans. This was suggested as having implications on future clinical applications especially for disorders where social interaction deficits are known eg. autism. Although some of these disorders are known to be linked to deficits in the neuronal mirror system, according to Tseng and colleagues they could also now be linked to ICS episodes. Therefore, further research was suggested as being advantageous since according to the authors it could lead to the possible development of a diagnostic tool, or as a measurement of ICS for monitoring of treatment, or as part of bioneurofeedback therapy for improving social motor skills.

COMMENT

What makes this article interesting is the link between one of the popular topics in the neurochemical world in today`s times, that of neuronal area connectivity, with one of the popular topics of ten to fifteen years ago, that of mirror neurons.  In this article, neuronal activity of particular motor learning areas is associated with movement and reward of one individual and observation of that movement and reward in another. This is somewhat different from the most of the mirror neuron work carried out previously where emotional status of the observer is essentially associated with a specific action and elicited emotion of the other active individual. Therefore, brain areas investigated in this article were the motor learning areas of the primary motor cortex (M1) known as responsible for the initiation and execution of actions and the dorsal pre-motor cortex (PMd or dorsal pre-motor area, PMA) linked with motivational input, sensorimotor integration and movement planning. The former area is not as well-known for mirror neuron activity as the latter. Tseng and colleagues took their discussion of mirror neurons in these areas further by looking at the relationship between the neuronal connectivity of the M1 and PMd within and between animals and attempted to associate periods of neuronal synchrony with examples of social interaction and social hierarchy observed in their experimental animals.

Two trains of thought relating to mirror neurons and brain area connectivity arise from the experiments carried out: the first train relates to brain area activity associated with motor movement and observation of that motor movement and why there should be periods of mirrored neuronal activity; and the second relates to the emotional status arising from the action and resulting reward or observation of them and whether this in anyway is reflected by the neuronal synchrony observed in the motor learning brain areas.

An investigation into the first train of thought leads automatically to the question as to what is actually happening in the M1 and PMd areas during the experiment. From a physical point of view what we have is essentially similar action from both observer and passenger in obtaining the reward eg. extension of the arm and grabbing plus eating, but there is a difference in motor movement before the reward is given. In essence the actual motor movement in this stage in both observer and passenger is the same. This can be explained by looking at how the experiment is set up. The observer is stationary with the passenger approaching (ie. no motor movement) and the passenger is stationary in the robotic chair (also the same, no motor movement ie. no climbing, no running) and therefore in this case the ´movement` being registered is a change of location and distance between it and the reward dispenser or other monkey. Therefore, neural activity in both M1 and PMd reflects the movements taking place before the reward and during the reward with some neural activity observed reflecting bottom-up input and control eg. incoming visual information, hand positioning and some top-down eg. the perception and interpretation of the situation, attention and emotional status.

At some points during the experimental time period according to the authors there are episodes of neuronal synchrony within the primary motor area (M1) and the pre-motor area (PMA) during the task that was carried out simultaneously with both monkeys. This would be expected in relation to the reward part of the task since both monkeys received the reward at the same time and therefore, activity in the PMA region would represent the planning of the actions required to obtain the reward and the activity in the M1 region would represent the movements actually being carried out. This would be the same for either monkey. With respect to the time before the rewards were given, then the periods of neuronal activity reflect the different situations of the monkeys (ie. the passenger moves, but the observer is stationary) and implies that the ability to register and interpret the actions of another requires activity in areas related to the motor system for both planning (eg SMA and PMA, M1) and execution (eg M1).  This goes against what we know since neither monkey actually executes the movements required to bring it closer to the other or its reward and therefore, for this time frame M1 activity should be minimal representing only the planning part of the task. It is the PMA where the most activity should be observed since it relates to the planning and intention of movement, which is not initiated. The M1 activity observed possibly reflects the suppression of movements since some neurons of the M1 are facilitators and others suppressors (their activity facilitates during only action observation). In the case of the passenger active movement is suppressed because the robotic chair brings him automatically to the reward and in the observer, active movement is suppressed because he is secured to a chair and can only observe, cannot initiate active movement and has to wait for the reward he knows will come as soon as his ´partner` carries out the required task ie. the distance between it and the grape dispenser is crossed.

The periods of neural synchrony observed were attributed by Tseng and colleagues to mirror neuron activity. As we have said above in the case of the reward this is understandable since both monkeys strive to reach the reward and then consume it. In the period before the reward, then periods of synchrony are also explainable. In the case of the PMA area, mirror neuron activity ie. neuronal firing activity which mirrors that of another`s performing the action is well known and this is said to be due to the area being responsible for motor movement rehearsal. The case of mirror neuron activity in the M1 is less known, but is still observed. Therefore, the periods of neural synchrony seen in the M1 and PMd areas between monkey passenger and monkey observer would represent those periods where both monkeys share the same informational input and demands regarding motor movement. Hence, periods of ICS would be expected when both monkeys received the reward for example. Periods of synchrony before the reward may reflect the intention of movement as described above which would be the same for both monkeys, or an alternative explanation is that the movement of the passenger monkey is mirrored by the perception of movement by the stationary observer monkey. This would be in the same way that a passenger on a stationary train that is passed by another train that is moving perceives movement. In the case of the monkeys performing the whole-body navigation task, the level of mirror neuron activity which is low anyway, may represent only a few features of the overall event that are shared and would be responsible for perception of the event. This explanation is possible since if learning has occurred the level of mirror neuron activity decreases with repetition of the tasks in the same way repeated real-life action does. However, in Tseng and colleagues experiments this does not occur. An explanation for this lack of modulation may be that the results quoted are amalgamations of test results and said to be the probability of incidences of neural synchrony and therefore, reductions of discharge rates for the areas may be obscured by the way the results are formulated. However, with regards to movement in this task it is more likely that mental imitation in the motor areas M1 and PMd represent task perception and planning before the reward and same or similar neural activity representing the same movements carried out relating to receiving and eating the reward.

This leads on then to question what is happening with regards to mirror neuron activity in the M1 and PMd areas in relation to social interaction as suggested by Tseng and colleagues. Social interaction in the monkey world reflects social hierarchical status and Tseng and his team demonstrated that the monkeys used in their experiments exhibited social standings which manifested into the amount of freedom of movement each monkey had, access to food, grooming etc. From a neurochemical perspective this social order would be learnt and learnt behaviour would follow the order. Deviations from the social order are interpreted as inducing, just like they would in humans, changes in the emotional system particularly fear.  For example, dominant monkey C is unlikely to experience fear if as passenger he approaches monkey J, the lowest monkey in the social order, but monkey J would (and also if he is in the passenger role). The activation of the fear system in this case would produce known changes in brain area activity eg. activation of the amygdala area  as well as changes in the quality and quantity of information inputted at the time and working memory and attentional system performances. Therefore, it is likely that in the case of the whole body navigation task behaviour not in keeping with social standing would result in a reduction of the periods of synchrony of neuronal activity observed since the activation of the fear system of the less dominant monkey would have induced changes in firing patterns to accommodate the situation the monkey found itself in. The brain areas affected appear not just to be those top-down areas such as involved in working memory, attention and decision making such as the ventromedial prefrontal cortex as expected, but also the brain areas relating to movement planning and execution. The role of the PMA, is understandable – fear or distress would instigate a greater level of movement planning for example to get the monkey out of the dangerous situation and since the M1 is also involved in planning activity, activity in this area would also likely to be increased. However, activity of these areas may not be synchronised to that observed in the more dominant monkey who does not experience fear. Therefore, it would be less likely that neural synchrony would be observed in times of high emotion.

Tseng and colleagues took the relationship between mirror neuron activity of the motor learning brain areas and social interaction further by suggesting that this relationship could be manipulated and controlled to help individuals suffering from disorders where social interaction is negatively affected. The interpretation of results here indicates that social skills of one individual can be learnt by mimicking the actions and emotional responses of another. From a neurochemical point of view an explanation for the mechanism required is relatively easy to formulate. The ´tutor` would perform the action with appropriate emotional and social responses which the ´observer` ie. the person learning would watch. According to Tseng and colleagues study, mirror neuron activity of the observer would elicit synchrony of the PMA firing and to a lesser effect the M1 area. Repetition of the action by the ´tutor` would mean that the PMA and M1 firing has the same pattern and so neuronal cell assemblies would be formed in the higher brain areas to represent both the action (whether a single event or a sequence) plus a positive emotional effect. A repeat of the action once learnt would then lead the observer to perform the appropriate action through reactivation of the past experience which would lead to the individual being able to perceive the situation, understand the situation and know from learnt behavioural examples how to react in what would be learnt and regarded as the proper manner. This method is known and forms the basis of many therapies eg. bioneurofeedback. However, it is probably not the panacea for all suitable therapies for this type of disorder since a factor to consider is the problem of transference of results and conclusions from a monkey which lives in a relatively simple social environment particularly those bred for scientific experiments to humans who live in a complex, constantly changing highly social environment. For example, the experiments by Tseng and colleagues do show a constraint on such learning since neuronal synchrony between the learner and ´tutor` would be reduced if either party was distressed and the emotional fear system was active. This would affect the level of learning and therefore, optimal learning would have to be carried out whilst the individuals were relaxed and mood was positively stable – a situation difficult to achieve and effectively monitor. Hence, the results of investigations such as these provide more knowledge about neurochemical processes, but they should not be directly transferred to humans and be applied to and influence social conditions.

Therefore, to conclude this comment on the positive side we can see that activity of brain areas associated with motor movement such as the M1 and PMA occurs when either an individual performs an action or observes an action, but the function of these activated areas could be different. In some cases, the neuronal activity of the M1 and PMA may be synchronised and this is said to be the work of mirror neurons of the observer brain. This could reflect shared features of active or observed events or reflect suppression or facilitation of firing. In one case the activity causes initiation and execution of the action; in the other the perception and interpretation of the action. The level of firing in the motor areas appears to be affected by emotional status and this is understandable in that the prefrontal cortex, basal ganglia, anterior cingulate cortex areas are all important components of not only the emotional system, but are also important in the motor loops responsible for bringing about motor movements.

Since we`re talking about the topic…………………………………………………….

…..would the substitution of pain instead of reward in the case of the observer substantiate Tseng and colleagues results relating to mirror neuron activity in the PMA and M1 regions when the observer was the less dominant of the pair, but cause a change when the more dominant became the observer?

……would the use of opposite arms and hands by the observer and passenger produce differences in neuronal activity in the PMd and M1 areas and decrease the number of neural synchrony episodes because of changes in the microzonal firing observed?

….can it be assumed that if the observer`s eyes were covered for part of the distance covered by the passenger in its route to the grape dispenser that PMd activity would remain since it can function in the absence of visual stimuli, but the episodes of neural synchrony between the observer and passenger during this time would decrease because the firing would represent different input?

 

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