Motor Cognition: TMS Studies of Action Generation Simone Schütz-Bosbach, Patrick Haggard, Luciano Fadiga and Laila Craighero
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30-Wasserman-Chap30 6/26/07 6:06 PM Page 463 CHAPTER 30 Motor cognition: TMS studies of action generation Simone Schütz-Bosbach, Patrick Haggard, Luciano Fadiga and Laila Craighero Introduction (e.g. Chapter 9, this volume). A TMS test pulse can provide a known, if artificial, input to the The discovery and earliest applications of TMS motor cortex. This will cause a twitch in target both involved the motor system (Barker et al. muscles (motor-evoked potential, MEP) whose 1985). Since then, TMS has been used in three amplitude can be precisely measured. It may quite different ways to study motor cognition. also cause an inhibition of ongoing electromyo- First, TMS can be used to provide a controllable gram (EMG) (silent period, SP). In cognitive- and physiologically-specified input to the skele- motor studies, the size of these excitatory or tomotor system. Several sensory studies, for inhibitory effects is measured as a function of example, have used TMS to generate muscle cognitive factors like task, expectancy and so contractions in the absence of volition and forth. Changes in the motor output for a con- movement preparation. This allows controlled stant TMS input are interpreted in terms of dif- psychophysical studies of the perception of bod- ferences between conditions, or across time, in ily movement (Haggard et al. 2002; Ellaway et al. motor system excitability. Importantly, this 2004; Haggard and Whitford 2004). In other method can provide a completely implicit and studies, TMS-evoked movements are used as on-line measure of the state of the cortical perturbations of the motor apparatus. Here the action system. Often a test pulse is preceded by focus is on preparatory and reactive adjustment a conditioning stimulus such as a sensory input for the perturbation (Bonnard et al. 2003 2004). or a conditioning TMS pulse to the same or In this method, TMS is generally delivered over another brain area. the primary motor cortex, but effects on the Third, TMS can be used to interfere with brain are less important than the effects on the cognitive-motor processes involved in action body. Although this use of TMS has great value control, and widely described throughout this as a peripheral stimulus for studying kinesthe- volume. Because the brain processes involved in sis, it is logically quite different from the use of generating a simple action are essentially serial, TMS to study specific brain areas and processes, a single TMS pulse delivered at an appropriate and so is not considered further here. time over an actively involved brain area may A second, very important use of TMS has disrupt action control. Such single-pulse effects been as an online probe of cortical motor tend to be highly informative, because of their excitability. This is reviewed in detail elsewhere temporal and spatial specificity. On the other 30-Wasserman-Chap30 6/26/07 6:06 PM Page 464 464 · CHAPTER 30 Motor cognition hand, their interpretation rests on a serial model of motor commands generating an appropriate of action control, which may not be sufficient movement pattern must be retrieved from the for all situations. Other studies have used off- many alternatives, thus achieving the desired line TMS effects, as a short-term virtual lesion. goal. This stage corresponds to the inverse This approach may be more powerful than sin- model or planner of computational models gle-pulse approaches, since it does not depend (Ghahramani et al. 1996). Preparation for on precisely timing a single pulse with respect to action then follows. This may involve further the underlying brain processes. However, by the elaboration of the motor command itself, but same token, it cannot clarify at what stage of the also more general anticipatory modulation of action control process a particular brain area reflex pathways and sensory areas likely to makes its contribution. receive afferent feedback as a result of the TMS allows the experimenter to selectively impending action (Voss et al. 2006). A key interfere with a specific brain process. It is there- moment in the serial control of action is the fore particularly adapted to testing serial models release of the motor command from the motor of cognitive processing (Donders 1868; Sternberg cortex, down the corticospinal tract (CT). The 1969). In these models, processing is assumed to corticospinal volley drives the actual contrac- occur in a serial sequence of independent tion of the muscles, and is the proximate cause modules, which implement distinct and inde- of the movement itself. This point therefore pendent operations. The successful completion marks the transition between action prepara- of each operation allows the next module to tion and action execution. For some very simple begin its operation. The value of these models is ‘ballistic’ actions, the model may be considered widely debated. Recent studies view the visual to stop here. In most cases, however, afferent system as a parallel rather than serial architecture, feedback from the moving effectors, and also involving multiple interconnected processing internal feedback from predictions based on streams (Milner and Goodale 1993). efference copy, are used to monitor the progress In contrast, the brain’s action system can be of the movement. Monitoring allows the motor viewed in two distinct ways. Voluntary actions command to be adjusted if it is incorrect, thus involve a clearly serial process (cf. Figure 30.1). reiterating the model. It also allows the success- Volition or intention can be seen as the input to ful completion of one movement to serve as the the process. These are followed by action selec- trigger for the next movement in a sequence. tion or specification. At this stage, a specific set Finally, action monitoring may be used for Fig. 30.1 A simple serial, hierarchical model of action control suitable for interpreting TMS studies. Note the increasing quantity and specificity of information as the action is elaborated. 30-Wasserman-Chap30 6/26/07 6:06 PM Page 465 Intentional actions and the serial model of action generation · 465 perceptual processes beyond the immediate and motivational states therefore constitute a motor control system, such as self-recognition reason for action. Neurophysiological evidence and agency (Haggard 2005). supports the existence of anatomical–functional Not all action research fits well with this serial links from the limbic system to premotor areas, model. Several neurophysiological, neuroimag- mediated by connections to the cingulated and ing and behavioral studies have focused on the prefrontal cortical regions. These earliest con- sensory guidance and internal representation of textual antecedents of action have proved diffi- action by a network of parietal and premotor cult to study with TMS for two reasons. First, regions (for a review see Freund et al. 2005). many motivational and limbic structures lie These studies focus on the transformation of deep within the brain and cannot be stimulated sensory representations into motor codes, and externally. Second, antecedent states such as the commonality between visual and motor rep- motivations and drives provide a tonic back- resentations of action. However, the results do ground to action rather than a single neural not always support a simple serial flow from event. They are not therefore amenable to investi- sensation to action. Neurophysiological and gation using phasic interventions such as TMS. neuroimaging results often reveal visual responses In one of the few TMS studies to investigate in ‘motor’ areas, while responses in early sensory action antecedents, Oliveri et al. (2003) used areas can show dramatic top-down modulation TMS to investigate the role of the supplemen- according to current motor task (Ruff et al. tary motor area (SMA) as a mediator between 2006). A recurrent feedback model may there- emotion and action. They accordingly measured fore be more appropriate than a strictly serial cortical excitability of primary motor cortex model for those sensorimotor actions that (M1) during processing of emotional versus involve relatively direct responses to environ- nonemotional visual stimuli. Subjects were mental stimuli. In the following we first review required to perform arbitrary movements in studies which can be situated within a simple response to unpleasant or neutral pictures of serial model of action generation. These studies people, animals or landscapes. The subjects have in common that they largely focus on the received a single TMS pulse over the left M1, control of voluntary or internally generated which was randomly preceded by paired TMS actions. Here TMS has predominantly been over the ipsilateral left SMA, left premotor cor- used as a technique to temporally disrupt spe- tex (PM) or right M1. The amplitudes of motor- cific cognitive processes at particular times. evoked potentials (MEPs) recorded from Second, we will discuss the use of TMS in subject’s right first dorsal interosseus (FDI) after research focusing on perception–action linkage, conditioning TMS were compared against those such as reaction and interaction with the envi- obtained after single TMS of the left M1. The ronment, including the social environment. In authors showed that conditioning TMS to SMA that tradition, parallel and interactive models selectively enhanced MEP amplitudes when dominate over serial models, but TMS has still subjects responded to emotionally unpleasant proved an important research tool, notably in pictures, and not when neutral visual cues were measuring cortical excitability. presented. However, conditioning TMS of PM or of the contralateral primary motor area did Intentional actions and the not show this effect. This finding confirms a specific functional link between SMA and pri- serial model of action mary motor areas in the control of movements generation that are triggered by emotional processing of certain visual cues. SMA seems to serve as a key Context and motivation for action area for transforming motivations, such as emo- Human action is generally goal-directed.