Motor Memory: Revealing Conditioned Action Tendencies Using Transcranial Magnetic Stimulation

Action tendencies can be elicited by motivationally salient stimuli (e.g., appetitive rewards) or objects that support utilization behaviors. These action tendencies can benefit behavioral performance through speeded RTs in response tasks and improve detection accuracy in attentional capture tasks. However, action tendencies can be counterproductive when goals change (e.g., refraining from junk foods or abstaining from alcohol). Maintaining control over cue-elicited action tendencies is therefore critical for successful behavior modification. To better understand this relationship, we used transcranial magnetic stimulation to investigate the neural signatures of action tendencies in the presence of previously trained response cues. Participants were presented with a continuous letter stream and instructed to respond quickly to two target letters using two different response keys. Following this training phase, the target letters were embedded in a new task (test phase), and we applied transcranial magnetic stimulation to the motor cortex and measured motor evoked potentials as an index of corticospinal excitability (CSE). We found that CSE could be potentiated by a former response cue trained within a single experimental session, even when participants were instructed to withhold responses during the test phase. Critically, attention to the previously trained response cue was required to elicit the primed modulation in CSE, and successful control of this activity was accompanied by CSE suppression. These findings suggest that well-trained response cues can come to prime a conditioned action tendency and provide a model for understanding how the implementation of cognitive control can override action automaticity.

[1]  Luigi Cattaneo,et al.  Broken affordances, broken objects: A TMS study , 2009, Neuropsychologia.

[2]  J. Gibson The Ecological Approach to Visual Perception , 1979 .

[3]  Kielan Yarrow,et al.  Are object affordances fully automatic? A case of covert attention. , 2013, Behavioral neuroscience.

[4]  T. Mima,et al.  Momentary reward induce changes in excitability of primary motor cortex , 2011, Clinical Neurophysiology.

[5]  Justin A. Harris,et al.  Motor-evoked potentials reveal functional differences between dominant and non-dominant motor cortices during response preparation , 2018, Cortex.

[6]  M. Costantini,et al.  The space of affordances: A TMS study , 2011, Neuropsychologia.

[7]  M Hallett,et al.  Human corticospinal excitability evaluated with transcranial magnetic stimulation during different reaction time paradigms. , 2000, Brain : a journal of neurology.

[8]  Aysha Keisler,et al.  Modulation of corticospinal excitability by reward depends on task framing , 2015, Neuropsychologia.

[9]  R. Ellis,et al.  Action priming by briefly presented objects. , 2004, Acta psychologica.

[10]  A. Mack,et al.  Potentiation of action by undetected affordant objects , 2008 .

[11]  R. Ellis,et al.  On the relations between seen objects and components of potential actions. , 1998, Journal of experimental psychology. Human perception and performance.

[12]  G. Petrovich,et al.  Learning and the motivation to eat: Forebrain circuitry , 2011, Physiology & Behavior.

[13]  Luca Turella,et al.  Corticospinal Facilitation during Observation of Graspable Objects: A Transcranial Magnetic Stimulation Study , 2012, PloS one.

[14]  R. Verleger,et al.  A TMS study on non-consciously triggered response tendencies in the motor cortex , 2006, Experimental Brain Research.

[15]  Dimitrios Kapogiannis,et al.  Reward‐related activity in the human motor cortex , 2008, The European journal of neuroscience.

[16]  Scott T. Grafton,et al.  Premotor Cortex Activation during Observation and Naming of Familiar Tools , 1997, NeuroImage.

[17]  E. Olivier,et al.  Influence of Reward on Corticospinal Excitability during Movement Preparation , 2012, The Journal of Neuroscience.

[18]  Carsten Bundt,et al.  Reward anticipation modulates primary motor cortex excitability during task preparation , 2016, NeuroImage.

[19]  Irina M. Harris,et al.  Automatic Recruitment of the Motor System by Undetected Graspable Objects: A Motor-evoked Potential Study , 2017, Journal of Cognitive Neuroscience.

[20]  K. Yarrow,et al.  The Truth-Telling Motor Cortex: Response Competition in M1 Discloses Deceptive Behaviour , 2011, Biological Psychology.

[21]  A. Aron,et al.  Top-Down Response Suppression Mitigates Action Tendencies Triggered by a Motivating Stimulus , 2014, Current Biology.

[22]  K L Shapiro,et al.  Temporary suppression of visual processing in an RSVP task: an attentional blink? . , 1992, Journal of experimental psychology. Human perception and performance.

[23]  K. Yarrow,et al.  Viewing objects and planning actions: On the potentiation of grasping behaviours by visual objects , 2011, Brain and Cognition.

[24]  Denis Cousineau,et al.  Confidence intervals in within-subject designs: A simpler solution to Loftus and Masson's method , 2005 .

[25]  W. Davis The Ecological Approach to Visual Perception , 2012 .

[26]  Michael Andres,et al.  Unsigned value prediction-error modulates the motor system in absence of choice , 2015, NeuroImage.

[27]  S. Bestmann,et al.  Time-Dependent Changes in Human Corticospinal Excitability Reveal Value-Based Competition for Action during Decision Processing , 2012, The Journal of Neuroscience.

[28]  Roshan Cools,et al.  Opposing Effects of Appetitive and Aversive Cues on Go/No-go Behavior and Motor Excitability , 2014, Journal of Cognitive Neuroscience.

[29]  M. Eimer,et al.  Effects of masked stimuli on motor activation: behavioral and electrophysiological evidence. , 1998, Journal of experimental psychology. Human perception and performance.

[30]  Pierre-Alexandre Klein,et al.  Comparison of the two cerebral hemispheres in inhibitory processes operative during movement preparation , 2016, NeuroImage.

[31]  A. Aron,et al.  Urges for food and money spill over into motor system excitability before action is taken , 2011, The European journal of neuroscience.

[32]  Eric-Jan Wagenmakers,et al.  Replication Bayes factors from evidence updating , 2018, Behavior Research Methods.

[33]  A. Aron,et al.  High Working Memory Load Increases Intracortical Inhibition in Primary Motor Cortex and Diminishes the Motor Affordance Effect , 2016, The Journal of Neuroscience.

[34]  H. Siebner,et al.  The Role of Pulse Shape in Motor Cortex Transcranial Magnetic Stimulation Using Full-Sine Stimuli , 2014, PloS one.