Selected Summaries

Neurophysiological basis of learning from error observation [PDF]

van Schie HT, Mars RB, Coles MGH, Bekkering H. (Nijmegen Institute for Cognition and Information, University of Nijmegen; F.C. Donders Centre for Cognitive Neuroimaging, Nijmegen, The Netherlands.) Modulation of activity in medial frontal and motor cortices during error observation. Nature Neurosci 2004;7:
549–54.

SUMMARY
Errors are crucial for learning and adjustment of behaviour. The discovery of the technique of recording error-related negativity (ERN) has helped to understand the neural basis of learning from errors. ERN, a component in the human event-related potential, is associated with activation of the anterior cingulate cortex (ACC), which is a part of the medial frontal cortex. The ACC was shown to be active during error correction. The role of the ACC was mostly studied under conditions where participants performed some tasks. However, learning of tasks and error correction can also occur during observation, a process that is considered to be crucial for the development of cognitive motor skills. This study was undertaken to test the hypothesis that the same neural mechanisms are active while learning during self-generated errors as well as observation of errors committed by others.
   Eighteen volunteers took part in a choice reaction task under two conditions. In one condition called ‘execution condition’, the volunteer performed the task. In the other condition called ‘observation condition’, the volunteer observed the experimenter performing the same task. In this second condition, the participant was referred to as the ‘observer’. The ERN and lateralized readiness potential (LRP) were recorded during both execution and observation conditions. During the choice reaction task, the electroencephalogram (EEG) of the volunteer was recorded from the scalp, to extract the ERN and LRP from the recordings. The EEG recordings were filtered out using an appropriate band pass for obtaining the ERN and LRP. The origins of ERN and LRP were localized by using the Brain Electric Source Analysis software.
     In the execution condition, there were larger negative deflections (i.e. ERNs) in the ACC during incorrect trials compared with correct trials. In the observation condition also, there were negative deflections (i.e. ERNs) during the incorrect trials. These data support the hypothesis that the medial frontal structures (i.e. ACC), involved in the processing of self-generated errors, are also activated during the observation of erroneous behaviour by others. The LRP initially showed a correct response in the observer’s motor cortex. Following the actor’s erroneous response, the observer’s motor system was activated differently.
    Thus, the study showed that the activities of the ACC and motor cortex were modulated by the correctness of both self-generated and observed responses. These areas may play a central role in observational learning.

COMMENT
Although committing an error is generally considered to be a negative event, errors are crucial for learning and adjusting future behaviour. This study found that activities in both the ACC and motor cortex were modulated not only by the correctness of one’s own actions, but were also altered, usually in a similar manner, even while observing the actions of others.

Brain regions involved in error-processing
The ACC is considered as a part of the neural network involved in reward-based selection for action.1 The ACC functions as a motor control filter, selecting appropriate responses from the available options. The existence of the error-processing system in the ACC has been inferred from ERN, a component of the event-related brain potential that is elicited when human participants commit errors in reaction-time tasks.2 Human functional imaging studies have shown that blood flow is increased in the ACC during performance under incompatible conditions. The ACC was activated more on error trials than correct ones.3

Techniques used in the study
The authors employed the Eriksen Flanker task in which subjects respond to stimuli by moving a joystick with their hand. Recording of event-related brain potentials (i.e. ERN and LRP) during performance of the task helped to investigate the neural mechanisms underlying error processing. Event-related brain potentials are small voltage fluctuations in the EEG, resulting from sensory or motor events. These electrical potentials are extracted from the spontaneous background scalp EEG with the help of computer averaging. Research on the neural processes underlying errors has been facilitated by the discovery of the ERN elicited during errors.4 When people make errors in a discrimination task, a negative-going waveform can be observed in a scalp-recorded EEG which is called the ERN. Dipole analysis has indicated that the origin of ERN is the ACC.5 The LRP is another event-related brain potential recorded in this study. This potential is considered to reflect motor activation, and has been used as a tool in elucidating the regions of the brain involved in the cognitive processes required to perform the task. During the performance of a task, the LRP starts after selection of the response hand and at the beginning of motor programming.

Implications of the study
Data from the present study suggest that the neural mechanisms used in the performance of a task are also activated under conditions of observation of the task. These mechanisms may play a central role in observational learning. Thus, the brain of the observer is activated in an almost similar manner as that of the person who performs the action. This has enormous implications in terms of learning and behaviour. Though it is generally accepted that learning can take place by the observation of action, this paper provides a neurophysiological basis for such learning.
   Though the motor cortex of the volunteers was activated during observation, their hand muscles were not. In fact, there was an active inhibition of muscle excitability to prevent overt replication of the action seen.6 There must be a mechanism which inhibits the hand muscles. It is not difficult to think of such a mechanism. Rapid eye movement (REM) sleep, which is associated with dreams, is characterized by increased cortical activity and the absence of muscle activity. The dreamer’s muscles would be totally relaxed even when he would be dreaming of vigorous muscle activity. This muscle atonia of REM sleep is due to the postsynaptic inhibition of spinal motor neurons resulting from the activation of a bulbospinal inhibitory system.7 In other words, there is a mechanism available in the brain that can prevent the execution of motor action. As we now have neurophysiological evidence of motor system activation during observation, further investigations may be required to study the brain mechanisms involved in preventing motor activity during the observation of action.
   This study provides scientific evidence that every observer also participates mentally in an observed action. The observed motor action may be moving a joystick, as in this study, or committing a heinous crime in a film that one is watching. It is important to emphasize that the observed behaviour of others provides a possible pathway for observational learning. Here, one is reminded of the statue of three monkeys, which was part of Mahatma Gandhi’s favoured collection. One of them was depicted as covering the mouth, the second covering the ears and the third covering the eyes. The message conveyed by this statue is that you should not say, hear or observe bad things. When you observe bad things, you mentally participate in the wrong act. Similarly, when you observe an error correction, you mentally participate in the corrective process.