PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. http://hdl.handle.net/2066/30141 Please be advised that this information was generated on 2021-10-02 and may be subject to change. Premotor contributions to the control of action: Selection, preparation, and monitoring ROGIER B. MARS F.C. DONDERS CENTRE FOR COGNITIVE NEUROIMAGING NIJMEGEN INSTITUTE FOR COGNITION AND INFORMATION RADBOUD UNIVERSITY NIJMEGEN The work described in this thesis was carried out at the F.C. Donders Cen- tre for Cognitive Neuroimaging. During this period, the promovendus was employed by the Nijmegen Institute for Cognition and Information, Faculty of Social Sciences, Radboud University Nijmegen. THESIS RADBOUD UNIVERSITEIT NIJMEGEN ISBN 90-9021103-9 COPYRIGHT c R.B. Mars, 2006 All rights reserved. No part of this publication may be reproduced, stored in a retrieval system, or transmitted, in any form, or by any means, electronic, mechanical, photocopying, recording, or otherwise, without the prior con- sent of the author. Printed in The Netherlands. INFORMATION P.O. Box 9104, 6500 HE Nijmegen, The Netherlands. E-mail: [email protected] DESIGN AND TYPESETTING Typeset with LATEX. PRINT Ipskamp, Enschede, The Netherlands. Premotor contributions to the control of action: Selection, preparation, and monitoring Een wetenschappelijke proeve op het gebied van de Sociale Wetenschappen PROEFSCHRIFT ter verkrijging van de graad van doctor aan de Radboud Universiteit Nijmegen op gezag van de Rector Magnificus prof. dr. C.W.P.M. Blom, volgens besluit van het College van Decanen in het openbaar te verdedigen op vrijdag 10 november 2006 des namiddags om 13.30 uur precies door Rogier Bertrand Mars geboren op 15 januari 1979 te Hengelo (Ov.) PROMOTORES: Prof. dr. M.G.H. Coles Prof. dr. W. Hulstijn COPROMOTOR: Dr. I. Toni MANUSCRIPTCOMMISSIE: Prof. dr. P. Hagoort Prof. dr. K.R. Ridderinkhof (University of Amsterdam) Dr. M.F.S. Rushworth (University of Oxford) Contents Contents v 1 Introduction 1 1.1 Voluntary action . 2 1.2 Movement preparation . 3 1.3 Action monitoring . 6 1.4 Premotor cortex . 10 1.5 Outline of this thesis . 14 2 Cerebral dynamics and topography of preparatory activity 17 2.1 Introduction . 18 2.2 Materials and methods . 19 2.3 Results . 26 2.4 Discussion . 31 3 On the programming and reprogramming of actions 35 3.1 Introduction . 36 3.2 Materials and methods . 37 3.3 Results . 42 3.4 Discussion . 45 4 Brain potentials and behavioral adjustments elicited by feed- back in a time-estimation task 49 4.1 Introduction . 50 4.2 Materials and methods . 51 4.3 Results . 53 4.4 Discussion . 55 5 Neural dynamics of error processing in medial frontal cortex 59 5.1 Introduction . 60 5.2 Materials and methods . 62 5.3 Results . 65 5.4 Discussion . 68 v CONTENTS 6 Modulation of activity in the premotor cortices during error observation 71 6.1 Introduction . 72 6.2 Materials and methods . 73 6.3 Results . 77 6.4 Discussion . 80 7 Discussion 83 7.1 Introduction . 84 7.2 Lateral premotor cortex . 84 7.3 Medial premotor cortex: Anterior cingulate cortex . 88 7.4 Medial premotor cortex: Pre-SMA and SMA proper . 92 7.5 Integration: Premotor contributions to the control of action . 95 Bibliography 97 Nederlandse samenvatting 115 De selectie en preparatie van acties . 115 Het evalueren van acties . 117 Het evalueren van het gedrag van anderen . 118 Discussie . 119 Acknowledgments 121 CV and publication list 125 Curriculum vitae . 125 Publication list . 125 Appendix: Color figures 129 vi 1 Introduction 1 1. INTRODUCTION 1.1 Voluntary action Humans display an almost endless repertoire of motor behavior. We breathe, walk in the garden looking at flowers, balance our posture during walking, stop to pick some flowers, decide to throw the yellow one away in favor of the red, retract a leg when stung by a bee, adjust our posture to provide some relief for the painful leg, and comment upon the complexity of life. These movements differ in the way in which we have voluntary control over them. Reflexes, such as retracting our leg when we feel pain being in- flicted, are a well-known example of movements over which we have almost no voluntary control. Habits, defined as movements that are so ‘overlearned’ that they have become involuntary and will be executed independent of the outcome of the response, are another such example. These reflexes and habits can be contrasted with actions over which we have full voluntary control (Dickinson, 1985). Our movement skills also differ in the way we acquire the ability to per- form them. Shadmehr and Wise (2005) distinguish three types of learning of motor skills, i.e., three types of motor learning. The first type is concerned with acquiring new motor skills during the course of evolution, through ran- dom mutations in a species’ genetic code and natural selection of adaptive mutations. Reflexes, such as retracting a limb when feeling pain from being stung by a bee, belong to the class of motor skills acquired through evolu- tion. The second type of motor learning is concerned with the acquisition of motor skills during the lifetime of an organism and maintaining a suit- able level of performance in response to changes. Within this type of motor learning, we can distinguish between skill acquisition and motor adapta- tion. Skill acquisition refers to learning how to perform a new motor action such as learning to walk. Motor adaptation refers to the ability to adapt the execution of a motor skill, such as learning to walk with an injured leg or, in a more experimental setting, learning how to make accurate reaching movements following the application of forcefield designed to consistently interfere with movements in a reaching paradigm (Shadmehr and Mussa- Ivaldi, 1994). The third type of motor learning concerns decision-making: learning which action to perform given a certain environmental input and knowing when to execute it. These different types of motor learning may rely on partly dissociable neural systems in the human brain (Brasted and Wise, 2005). The research presented in this thesis is concerned with the neural con- trol of voluntary actions. Passingham (1993) has defined these as actions that are made in the context of choosing among alternative, learned actions based on attention to those actions and their consequences. These are ac- tions over which we have full control, i.e. we can choose to execute or with- hold them depending on the circumstances, and which we have learned to perform during our lifetime. Therefore, voluntary actions as defined above fall into the third category of Shadmehr and Wise (2005). The question addressed in this thesis is: What is the role of a specific part of the human brain, the premotor cortex, in the selection and prepara- tion of voluntary actions and the evaluation of these actions following their 2 Movement preparation execution? The studies described focus on simple motor tasks, mostly employing arbitrary stimulus-response associations (Wise et al., 1996; Wise and Mur- ray, 2000). In these tasks the stimuli and the responses they instruct have no obvious (often spatial) relationship with one another, but are totally ar- bitrary and have to be learned. This type of stimulus-response mappings are at the core of the flexibility of the behavior of higher level animals and the ability of humans to respond to symbolic cuing of behavior (Wise and Murray, 2000). The remainder of this introductory chapter provides a framework for the studies discussed in Chapters 2-6. A review of the literature regarding the two specific action control processes that will be investigated in this thesis, namely motor preparation and performance monitoring, is given in the con- text of this framework. Furthermore, a brief review of the anatomy of the premotor cortex is provided. This chapter concludes with a brief overview of the rest of the thesis. 1.2 Movement preparation Planning a movement As described above, reflexive movements and habits will be executed when- ever the organism receives the appropriate stimulus. A reflex is thus a stereotypical movement. Parameters such as the goal of the action, e.g., preventing (further) harm to the organism, the part of the body to be moved, and the type of movement are all predetermined. In contrast, for voluntary actions the goals and preconditions for movement execution and the precise parameters of the movement are not predetermined and can vary accord- ing to task circumstances. This implies that a simple input-output model of the brain, in which all the brain does is transform the stimulus input to a motor output in a one-to-one mapping, is inadequate to describe the neural processes underlying voluntary actions (Jeannerod, 1997). Neural representations of various aspects of the voluntary action, including but not limited to the goal of the action, the internal state of the organism (e.g., hunger), the position of the limbs, and specific submovements of the action are necessary for the successful planning of voluntary actions. One of the challenges in the study of the neural control of actions is to investigate how these various aspects of a motor plan are represented in the brain, and how they are integrated in order to successfully select and execute a purposeful movement (Hikosaka et al., 1999; Willingham, 1998). Jeannerod (1997) postulates that these representations—together referred to as the movement representation—depend on sustained neuronal discharges arising in structures relevant to the various stages of the prepa- ration of motor acts. In accordance with this suggestion, a fruitful approach in studying the neural representations of action has been to record the ac- tivity of single neurons of the macaque brain while these monkeys perform variations of an instructed delay paradigm.