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Research Articles, Behavioral/Cognitive

Sensorimotor Expectations Bias Motor Resonance during Observation of Object Lifting: The Causal Role of pSTS

Guy Rens, Vonne van Polanen, Alessandro Botta, Mareike A. Gann, Jean-Jacques Orban de Xivry and Marco Davare
Journal of Neuroscience 13 May 2020, 40 (20) 3995-4009; https://doi.org/10.1523/JNEUROSCI.2672-19.2020
Guy Rens
1Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Biomedical Sciences Group, KU Leuven, Leuven, 3001, Belgium
2KU Leuven, Leuven Brain Institute, Leuven, 3001, Belgium
3The Brain and Mind Institute, University of Western Ontario, London, N6A 3K7 Ontario, Canada
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Vonne van Polanen
1Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Biomedical Sciences Group, KU Leuven, Leuven, 3001, Belgium
2KU Leuven, Leuven Brain Institute, Leuven, 3001, Belgium
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Alessandro Botta
4Department of Experimental Medicine, Section of Human Physiology, University of Genoa, Genoa, 16132, Italy
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Mareike A. Gann
1Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Biomedical Sciences Group, KU Leuven, Leuven, 3001, Belgium
2KU Leuven, Leuven Brain Institute, Leuven, 3001, Belgium
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Jean-Jacques Orban de Xivry
1Movement Control and Neuroplasticity Research Group, Department of Movement Sciences, Biomedical Sciences Group, KU Leuven, Leuven, 3001, Belgium
2KU Leuven, Leuven Brain Institute, Leuven, 3001, Belgium
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Marco Davare
5Department of Clinical Sciences and Centre for Cognitive Neuroscience, College of Health and Life Sciences, Brunel University London, Uxbridge, UB8 3PN, United Kingdom
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Abstract

Transcranial magnetic stimulation studies have highlighted that corticospinal excitability is increased during observation of object lifting, an effect termed “motor resonance.” This facilitation is driven by movement features indicative of object weight, such as object size or observed movement kinematics. Here, we investigated in 35 humans (23 females) how motor resonance is altered when the observer's weight expectations, based on visual information, do not match the actual object weight as revealed by the observed movement kinematics. Our results highlight that motor resonance is not robustly driven by object weight but easily masked by a suppressive mechanism reflecting the correctness of weight expectations. Subsequently, we investigated in 24 humans (14 females) whether this suppressive mechanism was driven by higher-order cortical areas. For this, we induced “virtual lesions” to either the posterior superior temporal sulcus (pSTS) or dorsolateral prefrontal cortex (DLPFC) before having participants perform the task. Importantly, virtual lesion of pSTS eradicated this suppressive mechanism and restored object weight-driven motor resonance. In addition, DLPFC virtual lesion eradicated any modulation of motor resonance. This indicates that motor resonance is heavily mediated by top-down inputs from both pSTS and DLPFC. Together, these findings shed new light on the theorized cortical network driving motor resonance. That is, our findings highlight that motor resonance is not only driven by the putative human mirror neuron network consisting of the primary motor and premotor cortices as well as the anterior intraparietal sulcus, but also by top-down input from pSTS and DLPFC.

SIGNIFICANCE STATEMENT Observation of object lifting activates the observer's motor system in a weight-specific fashion: Corticospinal excitability is larger when observing lifts of heavy objects compared with light ones. Interestingly, here we demonstrate that this weight-driven modulation of corticospinal excitability is easily suppressed by the observer's expectations about object weight and that this suppression is mediated by the posterior superior temporal sulcus. Thus, our findings show that modulation of corticospinal excitability during observed object lifting is not robust but easily altered by top-down cognitive processes. Finally, our results also indicate how cortical inputs, originating remotely from motor pathways and processing action observation, overlap with bottom-up motor resonance effects.

  • action observation
  • corticospinal excitability
  • mirror neurons
  • motor resonance
  • object lifting
  • sensorimotor
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The Journal of Neuroscience: 40 (20)
Journal of Neuroscience
Vol. 40, Issue 20
13 May 2020
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Sensorimotor Expectations Bias Motor Resonance during Observation of Object Lifting: The Causal Role of pSTS
Guy Rens, Vonne van Polanen, Alessandro Botta, Mareike A. Gann, Jean-Jacques Orban de Xivry, Marco Davare
Journal of Neuroscience 13 May 2020, 40 (20) 3995-4009; DOI: 10.1523/JNEUROSCI.2672-19.2020

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Sensorimotor Expectations Bias Motor Resonance during Observation of Object Lifting: The Causal Role of pSTS
Guy Rens, Vonne van Polanen, Alessandro Botta, Mareike A. Gann, Jean-Jacques Orban de Xivry, Marco Davare
Journal of Neuroscience 13 May 2020, 40 (20) 3995-4009; DOI: 10.1523/JNEUROSCI.2672-19.2020
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Keywords

  • action observation
  • corticospinal excitability
  • mirror neurons
  • motor resonance
  • object lifting
  • sensorimotor

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