Elsevier

Neuroscience

Volume 231, 12 February 2013, Pages 13-27
Neuroscience

The neural substrate of the ideomotor principle revisited: Evidence for asymmetries in action-effect learning

https://doi.org/10.1016/j.neuroscience.2012.11.035Get rights and content

Abstract

Ideomotor theory holds that the perception or anticipatory imagination of action effects activates motor tendencies toward the action that is known to produce these effects, herein referred to as ideomotor response activation (IRA). IRA presupposes that the agent has previously learned which action produces which effects, and that this learning process has created bidirectional associations between the sensory effect codes and the motor codes producing the sensory effects. Here, we refer to this process as ideomotor learning. In the presented fMRI study, we adopted a standard two-phase ideomotor learning paradigm; a mixed between/within-subjects design allowed us to assess the neural substrate of both, IRA and ideomotor learning. We replicated earlier findings of a hand asymmetry in ideomotor processing with significantly stronger IRA by left-hand than right-hand action effects. Crucially, we traced this effect back to more pronounced associative learning for action-contingent effects of the left hand compared with effects of the right hand. In this context, our findings point to the caudate nucleus and the angular gyrus as central structures of the neural network underlying ideomotor learning.

Highlights

► Investigation of brain activations underlying ideomotor (IM) processing by fMRI. ► In replication, IM response activation was increased for left-hand action effects. ► This hand asymmetry could be linked to an analogous asymmetry in IM learning. ► First description of the neural substrate of IM learning in the literature. ► Caudate nucleus and angular gyrus appeared as central structures of IM learning.

Introduction

The term ideo-motor was coined in the middle of the 19th century, at a time when Europe was captivated by alleged paranormal phenomena ascribed to transcendent powers like table turning or magical pendulums (Tischner, 1929). Carpenter (1882) tried to explain these phenomena by referring to unwilled and unconscious motor excitation elicited by the anticipatory imagination (“idea”) of a specific effect. For instance, thinking of a swinging or rotating pendulum may unconsciously trigger tiny muscle activation in the fingers which hold the pendulum and thereby produce the imagined motion: the “ideomotor reflex”.

Since then, the principle of triggering motor actions by effect anticipations has been embedded into a broad conceptual framework. Today, it is no longer seen as an involuntary reflex, bound to conditions of reduced will and expectant attention, but rather as a ubiquitous mechanism in voluntary action control – a truly executive function (James, 1890; see also Hommel et al., 2001, Pfister and Janczyk, 2012, Shin et al., 2010). In the following, we will refer to the mechanisms that relay sensory anticipations to motor centers as ideomotor response activation (IRA). This process relies on bidirectional associations between motor codes and sensory effect codes that have to be learned (Elsner and Hommel, 2001, Hoffmann et al., 2009). Once such action-effect associations have been acquired, activating a sensory effect code will automatically spread activation to the associated motor codes.

To put it in a broader theoretical framework, ideomotor assumptions can be related to general models of action control or limb praxis. One of the most influential theories of limb praxis was put forward by Rothi et al., 1991, Rothi et al., 1997, a two-route model which distinguishes between the performances of familiar or meaningful movements on the one hand and unfamiliar or meaningless movements on the other. The former and only these would recruit on the so-called “output praxicon”, a specialized long-term mnemonic structure which stores visuo-kinaesthetic attributes of movements, i.e. performance-related sensational or perceptual codes, which for movement execution are directly transcoded into motor programs. Entries of the output praxicon, in turn, get activated by more “passive” perceptual representations of physical characteristics (amplitude, spatial orientation, etc.) of actions, posited to be stored in another neurocognitive structure, the so-called “input praxicon”. According to the theory, the input praxicon allows to identify familiar actions of the agent’s repertoire, whereas the output praxicon supplies the motor implementation of actions at the innervatory pattern stage. Importantly, the outlined executive mechanism avoids the costs incurring for unfamiliar actions which require computing all the parameters needed to implement the spatial and temporal characteristics of intended movements (cf. Rothi and Heilman, 1996). There is an obvious similarity between the theoretically posited functionalities of output praxicon content on the one hand and learned action effects on the other, which are both assumed to be automatically transcoded into motor programs.

Similarly, ideomotor learning can be conceptualized as acquisition of a so-called inverse internal model (Wolpert and Kawato, 1998) which is a feedforward controller of motor action in which the output is identical to the input information. Basically, skillful coordinated limb movements arguably cannot be executed solely under feedback control, because feedback loops are generally slow and have small gains. Therefore, the brain needs to acquire an inverse dynamics model of intended action through motor learning, after which motor control can be executed in a pure feedforward manner (cf. Kawato, 1999, Wolpert and Ghahramani, 2000).

Whereas first neurophysiological studies have targeted the process of IRA (Elsner et al., 2002, Melcher et al., 2008, Kühn et al., 2011), the neural mechanisms underlying the preceding ideomotor learning are virtually unknown. Accordingly, the present study investigated the neural mechanisms underlying ideomotor learning and their relation to subsequent IRA.

To this end, we adopted a two-phase design that was previously used to assess the neurophysiological basis of IRAs (Melcher et al., 2008; cf. also Elsner and Hommel, 2001, Pfister et al., 2011). In an acquisition phase, participants performed key press actions to produce arbitrary action effects which in different subject groups were either contingent or non-contingent with the selected response. Thus, both groups had overall comparable sensory and motor activities but a different potential to exhibit ideomotor learning. In the subsequent test phase, participants of the contingency group were probed for IRA. Effect stimuli (i.e. stimuli which were presented as action effects during the acquisition phase) were now presented together with an imperative target stimulus1, which prompted participants either to freely choose a response or to withhold responding (Fig. 1). No-go trials of the latter kind allow defining the neural correlates of the perception of learned action effects independent of proper motor activation: the pure neural substrate of IRA (cf. Elsner et al., 2002, Melcher et al., 2008). The presence of go trials on the other hand increases the response readiness of subjects and thus assumably promotes effects of IRA during no-go trials2.

As outlined above, previous neurophysiological studies only investigated IRA (in more technical terms: the test phase) and neglected the underlying learning process (the acquisition phase). In these studies, IRA was mirrored in activity of the supplementary motor area (SMA) and the hippocampal system (Elsner et al., 2002, Melcher et al., 2008). The major goal of the present study was to investigate the learning process enabling such response activation effects. Interestingly, response activation effects in previous studies were entirely driven by structures associated with declarative memory such as the hippocampus or the parahippocampal gyrus. This medial temporal memory system is typically distinguished from a second, ‘habit learning system’ in the basal ganglia, i.e. comprising the putamen and caudate nucleus (e.g., Knowlton et al., 1996, Packard and Knowlton, 2002). Given that this second memory system was repeatedly associated with motor learning (see Seger, 2006, for a review), we expected ideomotor learning to draw on this system in addition to the medial temporal system (Tricomi et al., 2004).

Moreover, previous studies suggest that memory-based sensorimotor transformation or integration – i.e. output praxicon function (see above) – is represented in temporo-parietal regions. In this context, Peigneux et al. (2004), for instance, emphasized the contribution of the superior temporal cortex (superior temporal sulcus) in the sensory processing of action-related stimuli or proper motions. Rumiati et al. (2005) report a left-hemispherical pattern of increased activity comprising the inferior temporal gyrus and angular gyrus specifically in response to familiar actions, while Grèzes et al. (1999) related the inferior parietal cortex and the frontopolar cortex (FPC) to the acquisition of familiar actions during action observation (i.e. during visuomotor learning). Based on the outlined findings, ideomotor learning as a special instance of sensorimotor integration can be reasonably expected to rely on temporo-parietal regions in addition to genuine memory- or learning-related structures of the basal ganglia and the hippocampal system.

Furthermore, it is important to note that the described network for IRA found in previous studies only emerged for the left-hand but not for right-hand action-effects, indicating a fundamental asymmetry of ideomotor processes (cf. Melcher et al., 2008). Because the latter conclusion is based on ad hoc findings, it requires further empirical substantiation as well as theoretical elaboration and embedment. In this context, the Action-Perception model (Goodale and Milner, 1992, Milner and Goodale, 2010) emphasizes the differential skillfulness of left-hand and right-hand actions (which is based on the agent’s handedness) as a factor which could mediate their differential proneness to ideomotor processes. The rationale behind is that motor actions which are not highly skilled are controlled by the ventral stream in the same way as perception, whereas highly skilled or automated actions are controlled by the dorsal stream. This functional neuroanatomical similarity of motor and sensory processes assumably facilitates sensorimotor integration including ideomotor processes (cf. Wiediger and Fournier, 2008). However, if motor codes of less skillful left-hand actions are indeed more easily bound to sensory codes of perceived stimuli, this should concern not only IRA but ideomotor learning too. Accordingly, in the present fMRI study, we basically aimed at (1) replicating results of asymmetric IRA in a slightly modified design and (2) to test for analogous asymmetries in the underlying ideomotor learning process. More specifically, based on the results of our previous investigation, we expected to observe increased IRA-related brain activations for the left-hand compared to right-hand learned action effects particularly in medial temporal structures as well as in premotor and supplementary motor cortices. An analogous left-/right-hand side asymmetry for ideomotor learning was expected to occur likewise in activations of medial temporal structures as well as in activations of the basal ganglia.

Section snippets

Participants

Thirty-six healthy, right-handed participants were recruited from the local university’s student community. All subjects gave written-informed consent. They reported normal or corrected-to-normal vision, no history of psychiatric or neurological illness, and were currently not under psychotropic medication. Subjects were randomly assigned to one of the two experimental groups: 20 to the contingency group and 16 to the non-contingency group. Three subjects, however, had to be excluded from

Acquisition phase: neural substrate of action-effect association

Contrasts of the learning regressors are listed in Table 1 and particularly for left-hand action effects visualized in Fig. 2. In a nutshell, we found stronger activation decreases for contingent than for non-contingent action effects for both hands, but we did not observe any stronger activation increases. Contingent right-hand action effects showed a stronger decrease of brain activation in the rostral (perigenual) anterior cingulate cortex, reaching into the corpus callosum (t = 4.51;

Discussion

The present study investigated neural mechanisms that underlie ideomotor processing, particularly the acquisition of action-effect associations by ideomotor learning and the later activation of motor tendencies by the learned action effects (cf. Elsner et al., 2002, Melcher et al., 2008, Kühn et al., 2011).

To our knowledge, this is the first study to investigate the neural substrate of bidirectional action-effect learning. For this purpose, we used a time-by-condition interaction analysis that

Conclusions

In the present work, we investigated the neural mechanisms underlying ideomotor processing, i.e. the acquisition of action-effect associations (ideomotor learning) and the triggering of motor activation by the perception of learned action effects (IRA). We were able to replicate earlier findings of a hand asymmetry in IRA (significantly stronger for left-hand compared to right-hand learned action effects) which we traced back to an analogous hand asymmetry in ideomotor learning. Crucially, to

Acknowledgments

We thank Mr. Timo M.D. Graen (M. Sc. in Physics) for his highly competent support in the programming of the experimental stimulation. Moreover, we are grateful to two anonymous reviewers for their helpful comments and suggestions.

References (61)

  • T. Melcher et al.

    The neural substrate of the ideomotor principle: an event-related fMRI analysis

    NeuroImage

    (2008)
  • R. Pfister et al.

    Adaptive control of ideomotor effect anticipations

    Acta Psychol

    (2010)
  • I. Toni et al.

    Learning arbitrary visuomotor associations: temporal dynamic of brain activity

    NeuroImage

    (2001)
  • E.M. Tricomi et al.

    Feedback signals in the caudate reflect goal achievement on a declarative memory task

    NeuroImage

    (2008)
  • E.M. Tricomi et al.

    Modulation of caudate activity by action contingency

    Neuron

    (2004)
  • N.C. Voermans et al.

    Interaction between the human hippocampus and the caudate nucleus during route recognition

    Neuron

    (2004)
  • N.M. White et al.

    Multiple parallel memory systems in the brain of the rat

    Neurobiol Learn Mem

    (2002)
  • D.M. Wolpert et al.

    Multiple paired forward and inverse models for motor control

    Neural Netw

    (1998)
  • H. Burton et al.

    Tactile-vibration-activated foci in insular and parietal-opercular cortex studied with positron emission tomography: mapping the second somatosensory area in humans

    Somatosens Mot Res

    (1993)
  • R.M. Carelli et al.

    Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing task

    J Neurosci

    (1997)
  • Carpenter WB (1882) On the influence of suggestion in modifying and directing muscular movement, independently of...
  • I.B. Dutzi et al.

    The microgenesis of action-effect binding

    Psychol Res

    (2009)
  • F. Eippert et al.

    Blockade of endogenous opioid neurotransmission enhances acquisition of conditioned fear in humans

    J Neurosci

    (2008)
  • B. Elsner et al.

    Effect anticipation and action control

    J Exp Psychol Human

    (2001)
  • C. Farrer et al.

    The angular gyrus computes action awareness representations

    Cereb Cortex

    (2008)
  • G.R. Fink et al.

    Multiple nonprimary motor areas in the human cortex

    J Neurophysiol

    (1997)
  • S.D. Forman et al.

    Improved assessment of significant change in functional magnetic resonance imaging (fMRI): use of a cluster size threshold

    Magn Reson Med

    (1995)
  • S.T. Grafton et al.

    Motor sequence learning with the nondominant left hand. A PET functional imaging study

    Exp Brain Res

    (2002)
  • J. Grèzes et al.

    The effects of learning and intention on the neural network involved in the perception of meaningless actions

    Brain

    (1999)
  • J. Hoffmann et al.

    Movements or targets: what makes an action in action-effect learning?

    Q J Exp Psychol

    (2009)
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