Alpha oscillations reflect similar mapping mechanisms for localizing touch on hands and tools

Abstract

It has been suggested that our brain re-uses body-based computations to localize touch on tools, but the neural implementation of this process remains unclear. Neural oscillations in the alpha and beta frequency bands are known to map touch on the body in external and skin-centered coordinates, respectively. Here, we pinpointed the role of these oscillations during tool-extended sensing by delivering tactile stimuli to either participants' hands or the tips of hand-held rods. To disentangle brain responses related to each coordinate system, we had participants' hands/tool tips crossed or uncrossed at their body midline. We found that midline crossing modulated alpha (but not beta) band activity similarly for hands and tools, also involving a similar network of cortical regions. Our findings strongly suggest that the brain uses similar oscillatory mechanisms for mapping touch on the body and tools, supporting the idea that body-based neural processes are repurposed for tool use.

Keywords: Engineering; Neuroscience; Physics.

Graphical abstract

Figure 1

Experimental setup and paradigm Participants (n = 20) performed a tactile discrimination task for touches applied on two surfaces: (A) when applied on hands, participants hold their hands either in an uncrossed posture (left) or a crossed posture (right). (B) When applied on tools, participants hold tools either in an uncrossed posture (left) or a crossed posture (right) where only the tool tips crossed over the body midline (gray dotted line). (C) Trial structure of the tactile discrimination task: each trial started with the central cross blinking, followed by a spatial cue (half of the cross briefly turning blue) to indicate which side of space (left or right, equal probability) participants had to attend to. After a variable delay, tactile stimulation (here corresponding to time zero) was applied on participants’ right or left finger, or on the tip of the right or left rod, independently of the cued side. Tactile stimuli were either frequent standard stimuli (“single touch”, probability of 0.75), or rare deviant stimuli (“double touch”, probability of 0.25). Participants had to respond as fast and accurately as possible to rare tactile deviants presented to the cued side, and to ignore standard stimuli at the attended side, as well as all stimuli presented to the other side. (D) Total oscillatory activity of the post-stimulation period over contralateral somatosensory cortex (electrode C3) obtained from time-frequency decomposition using complex Morlet wavelets. Modulations are displayed as compared relative to baseline (−500 to −100 ms). Selected time windows for analysis are represented by gray rectangle for each frequency band: 250–500 ms for alpha and 150–300 ms for beta.

Figure 2

Alpha and beta activity after tactile stimulation (A) Topographies of alpha-band activity (8–13 Hz, 250 to 500 ms) in uncrossed (1st row) and crossed (2nd row) posture following unattended (1st column) and attended stimuli (2nd column). Difference topographies for attention effects in uncrossed and crossed posture (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. (B) Topographies of beta-band activity (15-25Hz, 150 to 300ms) in uncrossed (1st row) and crossed (2nd row) posture following unattended (1st column) and attended stimuli (2nd column). Difference topographies for attention effects in uncrossed and crossed posture (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. Data are displayed as if stimuli always occurred on the anatomically right hand or the tool held in the right hand, so that the left hemisphere is contralateral to tactile stimulation in a skin-based reference frame, independent of posture.

Figure 3

Alpha activity following tactile stimulation on the hand and on the tool (A) Topographies of alpha-band activity (8–13 Hz, 250 to 500 ms) when tactile stimuli happened on the hand, with uncrossed (1st row) and crossed (2nd row) hands following attended (1st column) and unattended (2nd column) stimuli. Different topographies for attention effects with uncrossed and crossed hands (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. (B) Topographies of alpha-band activity (8–13 Hz, 250 to 500 ms) when tactile stimuli happened on the tool, with uncrossed (1st row) and crossed hands (2nd row) following attended (1st column) and unattended (2nd column) stimuli. Different topographies for attention effects with uncrossed and crossed tools (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. (C) Source reconstruction of the interaction effect between attention and posture for tactile stimulation on the hand. (D) Source reconstruction of the interaction effect between attention and posture for tactile stimulation on the tool. Data are displayed as if stimuli always occurred on the anatomically right hand or tool held in the right hand, so that the left hemisphere is contralateral to tactile stimulation in a skin-based reference frame, independent of posture.

Figure 4

Alpha and beta activity after tactile stimulation in the right hemispace (A) Topographies of alpha-band activity (8–13 Hz, 250 to 500 ms) in uncrossed (1st row) and crossed (2nd row) posture following unattended (1st column) and attended stimuli (2nd column). Different topographies for attention effects in uncrossed and crossed posture (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. (B) Topographies of beta-band activity (15–25 Hz, 150 to 300 ms) in uncrossed (1st row) and crossed (2nd row) posture following unattended (1st column) and attended stimuli (2nd column). Different topographies for attention effects in uncrossed and crossed posture (3rd column), and for posture effects following attended and unattended stimuli (3rd row). Bottom-right corner: topography of the interaction between attention and posture. Data are displayed as if stimuli always occurred on the hand or tool localized in the right hemispace, independent of posture.