Sensory information from a slipping object elicits a rapid and automatic shoulder response

Abstract

Humans have the remarkable ability to hold, grasp, and manipulate objects. Previous work has reported rapid and coordinated reactions in hand and shoulder muscles in response to external perturbations to the arm during object manipulation; however, little is known about how somatosensory feedback of an object slipping in the hand influences responses of the arm. We built a handheld device to stimulate the sensation of slipping at all five fingertips. The device was integrated into an exoskeleton robot that supported it against gravity. The setup allowed us to decouple somatosensory stimulation in the fingers from forces applied to the arm, two variables that are highly interdependent in real-world scenarios. Fourteen participants performed three experiments in which we measured their arm feedback responses during slip stimulation. Slip stimulations were applied horizontally in one of two directions, and participants were instructed to either follow the slip direction or move the arm in the opposite direction. Participants showed shoulder muscle responses within ∼67 ms of slip onset when following the direction of slip but significantly slower responses when instructed to move in the opposite direction. Shoulder responses were modulated by the speed but not the distance of the slip. Finally, when slip stimulation was combined with mechanical perturbations to the arm, we found that sensory information from the fingertips significantly modulated the shoulder feedback responses. Overall, the results demonstrate the existence of a rapid feedback system that stabilizes handheld objects. NEW & NOTEWORTHY We tested whether the sensation of an object slipping from the fingers modulates shoulder feedback responses. We found rapid shoulder feedback responses when participants were instructed to follow the slip direction with the arm. Shoulder responses following mechanical joint perturbations were also potentiated when combined with slipping. These results demonstrate the existence of fast and automatic feedback responses in the arm in reaction to sensory input to the fingertips that maintain grip on handheld objects.

Mapping the integration of sensory information across fingers in human sensorimotor cortex

“…Although BA 4 is traditionally viewed as a motor area, it receives substantial inputs from the somatosensory thalamus (Jones, 1975;Darian-Smith & Darian-Smith, 1993) and from various areas of S1 (Ghosh, Brinkman, & Porter, 1987). Therefore, neural populations in this region may also be involved in integrating tactile inputs from the fingers, perhaps for rapid behavioural responses to object displacements (Crevecoeur et al, 2017;Hernandez-Castillo et al, 2020). Our results demonstrate that there were finger interactions in BA 4, and the strength of these interactions were comparable to those in BA 2.…”

“…Such modulation is important, as the processing requirements of somatosensory information depends on the task at hand. For example, the reaction to object slip depends not only on the direction of the slipping object (Häger-Ross, Cole, & Johansson, 1996), but also on the perceived physical properties of the object (i.e., how "object-like" the simulation is, Ohki, Edin, & Johansson, 2002), and the behavioural goal (Hernandez-Castillo et al, 2020). We may therefore expect that, in order to provide support for flexible sensory-motor mapping, the way that information is integrated across fingers changes with the behavioral context.…”

Bodily skill

“…Interestingly, this model of the arm appears to go beyond arm-muscle reflexes, and to flexibly integrate feedback from cutaneous receptors in the hand, as well as to direct feedback responses in conditions of fine grip control (Crevecour et al 2016, Forgaard et al 2021). So, for example, Hernandez-Castillo et al (2020) applied stimulus to the fingertips, mimicking an object slipping out of hand, and also applied stimulus to the shoulder, jostling the arm. Stimulus to the fingertips generated a long-latency reflex at the shoulder -the reflex aimed to move the arm in the direction of the falling object.…”

The role of feedback in the production of skilled finger sequences

“…When we grasp a full cup and feel a sudden slip, we can swiftly adjust our grip force to avoid the cup slipping from our hand. This correction can occur in less than 100 ms (Cole and Abbs 1988;Hernandez-Castillo et al 2020;Johansson et al 1992). Feedback from other senses such as vision (Day and Lyon 2000;Veerman et al 2008) and audition (Burnett et al 1998;Howell 2004) is also used for the control of an ongoing movements, albeit at slightly slower speeds (at 90-260 ms and 100-200 ms respectively).…”