Opinion
Prediction of external events with our motor system: towards a new framework

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We cannot, in the proper sense, imitate or re-enact inanimate events, such as ocean waves rolling, or even non-human animate ones, such as dogs walking. However, we can anticipate the way they change and recent studies show that our motor system becomes involved while doing so. A novel framework is presented that accounts for these findings by generalizing a predictive account of the motor system from action to event perception. It is suggested that we predict events that we cannot reproduce ourselves by exploiting an audiomotor or visuomotor representation that never amounts to a real action because it lacks proprioceptive and other interoceptive information. This view inspires thinking beyond our customary conceptualization of a ‘motor’ system.

Introduction

Events involve change, and change is often brought about by living entities. The question of how we predict the actions of conspecifics has been the source of widespread scientific interest and has also inspired several recent investigations in the cognitive neurosciences 1, 2, 3. An exciting answer to this question stems from the concept of simulation (Box 1, Figure I). According to this view, we predict what others are doing by using our own motor system as an internal model or ‘emulator’. It is suggested that motor activation triggered by action observation feeds back into perceptual processing, creating top-down expectations and constraining predictions [4].

However, this account does not explain how we are able to predict the actions of other animal species. Moreover, it cannot explain how we deal with other types of changes, namely those generated by inanimate events, caused by machines or natural forces. So how do we predict events that we cannot properly incorporate into our motor system? Recently, the principle of simulation has been proposed to account for diverse predictive phenomena in human perception and cognition [5]. What remains to be seen is how those simulations are realized in the brain, particularly those that do not seem to be nested in the domain of motor control. Even relatively simple types of object motion seem to call upon higher-order processes [6], such as internal models of gravity for the perception of falling objects [7]. However, daily experienced events involve more complex patterns of changes and many of them, including most auditory events, are not defined merely by motion. Yet, when we attend to them, we can predict their outcomes to a reasonable extent. For instance, when observing a flying insect, we set up specific expectations about the flying pattern depending on whether the insect is a fly, bee, butterfly or beetle. And if we lie in the dark and listen to the sound of a mosquito, auditory prediction can estimate when and where it has landed.

The present article puts forward the hypothesis that predictive accounts of the sensorimotor system can be generalized from action to event perception. I propose that we use our sensorimotor system by default in a simulation mode for predictions of observable events of any kind as long as they take place within several seconds. This view will be outlined in detail over the following sections. It is based on experimental evidence that shows that the prediction of different styles of changes not only draws on the sensorimotor system but also requires an intact sensorimotor system. Perhaps most strikingly, we effectively use our sensorimotor system to simulate events that we – principally or contingently – cannot reproduce or imitate. The patterns of activation revealed by imaging studies provide the basis for this proposal concerning how our sensorimotor system qualifies to serve event prediction.

Section snippets

Evidence for a premotor role in event prediction

In a recent series of functional magnetic resonance imaging (fMRI) studies, we investigated the neural correlates of prediction [8] (Box 2) and showed that predictions of abstract events engage our motor system, particularly the premotor cortex and its parietal projection areas (e.g. Refs 9, 10, 11, 12, 13, 14; for a meta-analysis of related imaging findings, see Ref. [15]). Patient data [16] and repetitive transcranial magnetic stimulation data [17] rule out the possibility that motor

How much re-enactment is required for simulation?

The ability to reproduce what we see or hear has an influence on the sensorimotor system, as demonstrated in studies that compare action experts and novices 18, 19, 20, 21. The accuracy of prediction is a function of how closely an observed action and one's own ability to produce this action are related 22, 23. In terms of internal models, one might say that, in the case of movements we can reproduce, we use our motor memories to run a simulation of the observed movement (Box 1, Figure II).

Predicting events we cannot reproduce

When we listen to a melody repeatedly, the lateral premotor cortex establishes sensorimotor representations (it can be suggested that this process is implemented by unsupervised learning [25]), using the input provided by the parietal and temporal association cortex (Figure 1a). (See Ref. [26] for sensorimotor integration and transformation in premotor–parietal loops.) The ‘motor’ part of the sensorimotor representation does not amount to a movement that, when executed, leads to the sensory

Suggestions on the cerebral implementation of event prediction

A possible answer to this question is provided by the Habitual Pragmatic Event Map (HAPEM; formerly Habitual Pragmatic Body Map) framework [15], which is based on imaging findings (Box 2). The HAPEM framework holds that, by default, the prediction of an event that is structured with regard to a property P engages the area of the lateral premotor cortex that is best adapted to specify its motor output in terms of property P. Let us consider ocean waves rolling iteratively on the shore. Their

Internal models of events: a neuroanatomical classification

Conceptually, it would be useful to have a terminology that describes the role of the premotor cortex in the simulation of action and in the simulation of events in a unifying framework. This should be possible because forward models for events are not categorically different from forward models for actions. Forward models for events are just a fraction of forward models for actions, a fraction that misses the full-blown interoceptive and exteroceptive description of action models. A term is

Implications on motor imagery, action perception and the human sensorimotor system

Motor imagery cannot account for event prediction. Although, in mental rotation, it might be appropriate to assume that motor areas ‘are active in producing motor commands of the sort that would lead to the overt counterpart of the imagined event’ ([5], p. 387), this formula is misleading when generalized to event prediction. It implies that we possess a complete representation of all expected sensory consequences of an action that amount to the observed event, which in most cases is

Concluding remarks

Currently, there is much discussion about how cognition might be rooted in ‘motor’- and ‘body’-related functions (e.g. embodiment and re-enactment; e.g. Refs 37, 38, 39). The current paper has outlined the idea that a predictive account of the motor system can be generalized from action to events and has described how simulation of events can be realized in our sensorimotor system. According to this view, prediction of events is achieved by the aid of sensorimotor-driven forward models. Note

Acknowledgements

Thanks to Andrea Gast-Sandmann and Kerstin Flake for support in preparing figures and boxes, and Anna Abraham, Uta Wolfensteller, Andreja Bubic, D.Y. von Cramon and Kirsten G. Volz for many helpful comments and proofreading.

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