Sensorimotor expectations bias motor resonance during observation of object lifting: The causal role of pSTS

AbstractTranscranial magnetic stimulation (TMS) studies have highlighted that corticospinal excitability (CSE) 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 the 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) prior to 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. Altogether, 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 StatementObservation 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 to 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.

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Virtual lesion of right posterior superior temporal sulcus modulates conscious visual perception of fearful expressions in faces and bodies

Cortex ◽

10.1016/j.cortex.2015.01.012 ◽

2015 ◽

Vol 65 ◽

pp. 184-194 ◽

Cited By ~ 16

Author(s):

Matteo Candidi ◽

Bernard M.C. Stienen ◽

Salvatore M. Aglioti ◽

Beatrice de Gelder

Keyword(s):

Visual Perception ◽

Superior Temporal Sulcus ◽

Virtual Lesion ◽

Posterior Superior Temporal Sulcus

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Learning to See Biological Motion: Brain Activity Parallels Behavior

Journal of Cognitive Neuroscience ◽

10.1162/0898929042568569 ◽

2004 ◽

Vol 16 (9) ◽

pp. 1669-1679 ◽

Cited By ~ 85

Author(s):

Emily D. Grossman ◽

Randolph Blake ◽

Chai-Youn Kim

Keyword(s):

Neural Activity ◽

Biological Motion ◽

Brain Activity ◽

Daily Practice ◽

Superior Temporal Sulcus ◽

Fusiform Face Area ◽

Face Area ◽

Perceptual Performance ◽

Trained Observers ◽

Posterior Superior Temporal Sulcus

Individuals improve with practice on a variety of perceptual tasks, presumably reflecting plasticity in underlying neural mechanisms. We trained observers to discriminate biological motion from scrambled (nonbiological) motion and examined whether the resulting improvement in perceptual performance was accompanied by changes in activation within the posterior superior temporal sulcus and the fusiform “face area,” brain areas involved in perception of biological events. With daily practice, initially naive observers became more proficient at discriminating biological from scrambled animations embedded in an array of dynamic “noise” dots, with the extent of improvement varying among observers. Learning generalized to animations never seen before, indicating that observers had not simply memorized specific exemplars. In the same observers, neural activity prior to and following training was measured using functional magnetic resonance imaging. Neural activity within the posterior superior temporal sulcus and the fusiform “face area” reflected the participants' learning: BOLD signals were significantly larger after training in response both to animations experienced during training and to novel animations. The degree of learning was positively correlated with the amplitude changes in BOLD signals.

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Generalization of motor learning in psychological space

10.1101/2021.02.09.430542 ◽

2021 ◽

Cited By ~ 1

Author(s):

Eugene Poh ◽

Naser Al-Fawakari ◽

Rachel Tam ◽

Jordan A. Taylor ◽

Samuel D. McDougle

Keyword(s):

Motor Learning ◽

Human Behavior ◽

Visuomotor Adaptation ◽

Movement Kinematics ◽

Top Down ◽

Target Shape ◽

Motor Behaviors ◽

Inference Problems ◽

Similarity Ratings ◽

High Level

ABSTRACTTo generate adaptive movements, we must generalize what we have previously learned to novel situations. The generalization of learned movements has typically been framed as a consequence of neural tuning functions that overlap for similar movement kinematics. However, as is true in many domains of human behavior, situations that require generalization can also be framed as inference problems. Here, we attempt to broaden the scope of theories about motor generalization, hypothesizing that part of the typical motor generalization function can be characterized as a consequence of top-down decisions about different movement contexts. We tested this proposal by having participants make explicit similarity ratings over traditional contextual dimensions (movement directions) and abstract contextual dimensions (target shape), and perform a visuomotor adaptation generalization task where trials varied over those dimensions. We found support for our predictions across five experiments, which revealed a tight link between subjective similarity and motor generalization. Our findings suggest that the generalization of learned motor behaviors is influenced by both low-level kinematic features and high-level inferences.

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A region of right posterior superior temporal sulcus responds to observed intentional actions

Neuropsychologia ◽

10.1016/j.neuropsychologia.2004.04.015 ◽

2004 ◽

Vol 42 (11) ◽

pp. 1435-1446 ◽

Cited By ~ 253

Author(s):

R Saxe ◽

D.-K Xiao ◽

G Kovacs ◽

D.I Perrett ◽

N Kanwisher

Keyword(s):

Superior Temporal Sulcus ◽

Intentional Actions ◽

Posterior Superior Temporal Sulcus

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Rostro‐caudal organization of the human posterior superior temporal sulcus revealed by connectivity profiles

Human Brain Mapping ◽

10.1002/hbm.24349 ◽

2018 ◽

Vol 39 (12) ◽

pp. 5112-5125 ◽

Cited By ~ 1

Author(s):

Chen Cheng ◽

Lingzhong Fan ◽

Xiaoluan Xia ◽

Simon B. Eickhoff ◽

Hai Li ◽

...

Keyword(s):

Superior Temporal Sulcus ◽

Posterior Superior Temporal Sulcus

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Motor Resonance May Originate From Sensorimotor Experience

Journal of Neurophysiology ◽

10.1152/jn.00386.2010 ◽

2010 ◽

Vol 104 (4) ◽

pp. 1867-1871 ◽

Cited By ~ 23

Author(s):

Agustín Petroni ◽

Federico Baguear ◽

Valeria Della-Maggiore

Keyword(s):

Motor System ◽

Motor Evoked Potentials ◽

Human Subjects ◽

Action Observation ◽

Physical Nature ◽

Corticospinal Excitability ◽

Motor Resonance ◽

Major Interest ◽

Movement Index ◽

Static Pictures

In humans, the motor system can be activated by passive observation of actions or static pictures with implied action. The origin of this facilitation is of major interest to the field of motor control. Recently it has been shown that sensorimotor learning can reconfigure the motor system during action observation. Here we tested directly the hypothesis that motor resonance arises from sensorimotor contingencies by measuring corticospinal excitability in response to abstract non-action cues previously associated with an action. Motor evoked potentials were measured from the first dorsal interosseus (FDI) while human subjects observed colored stimuli that had been visually or motorically associated with a finger movement (index or little finger abduction). Corticospinal excitability was higher during the observation of a colored cue that preceded a movement involving the recorded muscle than during the observation of a different colored cue that preceded a movement involving a different muscle. Crucially this facilitation was only observed when the cue was associated with an executed movement but not when it was associated with an observed movement. Our findings provide solid evidence in support of the sensorimotor hypothesis of action observation and further suggest that the physical nature of the observed stimulus mediating this phenomenon may in fact be irrelevant.

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