Seeing your own or someone else's hand moving in accordance with your action: The neural interaction of agency and hand identity

Abstract

Forward models can predict sensory consequences of self-action, which is reflected by less neural processing for actively than passively generated sensory inputs (BOLD suppression effect). However, it remains open whether forward models take the identity of a moving body part into account when predicting the sensory consequences of an action. In the current study, fMRI was used to investigate the neural correlates of active and passive hand movements during which participants saw either an on-line display of their own hand or someone else's hand moving in accordance with their movement. Participants had to detect delays (0-417 ms) between their movement and the displays. Analyses revealed reduced activation in sensory areas and higher delay detection thresholds for active versus passive movements. Furthermore, there was increased activation in the hippocampus, the amygdala, and the middle temporal gyrus when someone else's hand was seen. Most importantly, in posterior parietal (angular gyrus and precuneus), frontal (middle, superior, and medial frontal gyrus), and temporal (middle temporal gyrus) regions, suppression for actively versus passively generated feedback was stronger when participants were viewing their own compared to someone else's hand. Our results suggest that forward models can take hand identity into account when predicting sensory action consequences. K E Y W O R D Sagency, fMRI, forward model, hand identity, hand movement, prediction, self-other

Transcranial direct current stimulation improves action-outcome monitoring in schizophrenia spectrum disorder

“…The sensory outcomes of one’s own actions are usually highly predictable, and small temporal violations of expected action-outcome associations can be detected with relative ease by healthy participants ( van Kemenade et al , 2016 , 2017 , 2019 b ; Schmalenbach et al , 2017 ; Straube et al , 2017 b ; Arikan et al , 2019 ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). These predictive mechanisms allow us to anticipate the future state of both the environment and ourselves to compensate for delays in the transmission of neural signals and to conserve resources by suppressing the processing of self-generated stimuli when they match our predictions ( Straube et al , 2017 b ).…”

“…by rotating visual feedback of the hand ( Farrer et al , 2003 ; Synofzik et al , 2010 ) or are temporally remapped, e.g. by delaying visual and/or auditory feedback ( Blakemore et al , 2001 ; Hashimoto and Sakai, 2003 ; Leube et al , 2003 , 2010 ; Farrer et al , 2008 ; Kurayama et al , 2012 ; Backasch et al , 2014 ; van Kemenade et al , 2016 , 2017 , 2019 b ; Schmalenbach et al , 2017 ; Straube et al , 2017 b ; Arikan et al , 2019 ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). In addition to these voluntary conditions, passive and/or unpredictable control conditions, such as externally generated/passive movements, have been studied ( Blakemore et al , 1998 , 1999 , 2000 b ; Arikan et al , 2019 ; van Kemenade et al , 2019 b ; Pazen et al , 2020 ; Uhlmann et al , 2020 ).…”

“…by delaying visual and/or auditory feedback ( Blakemore et al , 2001 ; Hashimoto and Sakai, 2003 ; Leube et al , 2003 , 2010 ; Farrer et al , 2008 ; Kurayama et al , 2012 ; Backasch et al , 2014 ; van Kemenade et al , 2016 , 2017 , 2019 b ; Schmalenbach et al , 2017 ; Straube et al , 2017 b ; Arikan et al , 2019 ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). In addition to these voluntary conditions, passive and/or unpredictable control conditions, such as externally generated/passive movements, have been studied ( Blakemore et al , 1998 , 1999 , 2000 b ; Arikan et al , 2019 ; van Kemenade et al , 2019 b ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). Delay-detection tasks, in which a lengthened interval between one’s own action and the resulting perceptual consequences has to be detected, have been used in several studies focusing on temporal outcome prediction ( Hashimoto and Sakai, 2003 ; Leube et al , 2003 , 2010 ; Farrer et al , 2008 ; van Kemenade et al , 2016 , 2019 a ; Straube et al , 2017 b ; Pazen et al , 2020 ; Uhlmann et al , 2020 ).…”

“…In addition to these voluntary conditions, passive and/or unpredictable control conditions, such as externally generated/passive movements, have been studied ( Blakemore et al , 1998 , 1999 , 2000 b ; Arikan et al , 2019 ; van Kemenade et al , 2019 b ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). Delay-detection tasks, in which a lengthened interval between one’s own action and the resulting perceptual consequences has to be detected, have been used in several studies focusing on temporal outcome prediction ( Hashimoto and Sakai, 2003 ; Leube et al , 2003 , 2010 ; Farrer et al , 2008 ; van Kemenade et al , 2016 , 2019 a ; Straube et al , 2017 b ; Pazen et al , 2020 ; Uhlmann et al , 2020 ). These tasks focus the participant’s attention on the perceptual consequences of an action and provide a direct behavioural measure of the function of interest, namely the comparison of predicted and perceived time points of sensory information.…”

Measures of agency

“…Furthermore, one can assume that these predictive mechanisms rely on different types of learned associations, as well as different types of associative strength. This kind of difference between a comparator mechanism for movement and for distal effects has been confirmed by a recent fMRI study by Uhlmann et al (2020) indicating that recognition of one’s own hand rely on information specifying hand identity. Prior establishment of hand identity is not needed when the brain computes a sense of agency for the movement.…”