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Coding and use of tactile signals from the fingertips in object manipulation tasks

Key Points

  • Object manipulation tasks comprise sequentially organized action phases that are generally delineated by distinct mechanical contact events representing task subgoals. To achieve these subgoals, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output in anticipation of requirements imposed by objects' physical properties.

  • Crucial control operations are centred on events that mark transitions between action phases. At these events, the CNS both receives and makes predictions about sensory information from multiple sources. Mismatches between predicted and actual sensory outcomes can be used to quickly and flexibly launch corrective actions as required.

  • Signals from tactile afferents provide rich information about both the timing and the physical nature of contact events. In addition, they encode information related to object properties, including the shape and texture of contacted surfaces and the frictional conditions between these surfaces and the skin.

  • A central question is how tactile afferent information is encoded and processed by the brain for the rapid detection and analysis of contact events. Recent evidence suggests that the relative timing of spikes in ensembles of tactile afferents provides such information fast enough to account for the speed with which tactile signals are used in object manipulation tasks.

  • Contact events in manipulation can also be represented in the visual and auditory modalities and this enables the brain to simultaneously evaluate sensory predictions in different modalities. Multimodal representations of subgoal events also provide an opportunity for the brain to learn and uphold sensorimotor correlations that can be exploited by action-phase controllers.

  • A current challenge is to learn how the brain implements the control operations that support object manipulations, such as processes involved in detecting sensory mismatches, triggering corrective actions, and creating, recruiting and linking different action-phase controllers during task progression. The signal processing in somatosensory pathways for dynamic context-specific decoding of tactile afferent messages needs to be better understood, as does the role of the descending control of these pathways.

Abstract

During object manipulation tasks, the brain selects and implements action-phase controllers that use sensory predictions and afferent signals to tailor motor output to the physical properties of the objects involved. Analysis of signals in tactile afferent neurons and central processes in humans reveals how contact events are encoded and used to monitor and update task performance.

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Figure 1: Encoding of fingertip force direction and contact surface shape.
Figure 2: Corrective actions triggered by a mismatch between predicted and actual sensory events.
Figure 3: Hypothetical model for the fast processing of afferent information in somatosensory pathways.
Figure 4: Visual and tactile control points in a manipulation task.

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Acknowledgements

The Swedish Research Council (project 08667), the sixth Framework Program of the EU (project IST-028056), and the Canadian Institutes of Health Research supported this work.

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Correspondence to Roland S. Johansson.

Glossary

Tactile afferents

Fast-conducting myelinated afferent neurons that convey signals to the brain from low-threshold mechanoreceptors in body areas that actively contact objects — that is, the inside of the hand, the sole of the foot, the lips, the tongue and the oral mucosa.

Proprioceptive afferents

Fast-conducting myelinated afferents that provide information about joint configurations and muscle states. These include mechanoreceptive afferents from the hairy skin, muscles, joints and connective tissues.

Action-phase controller

A learned sensorimotor 'control policy' that uses specific sensory information and sensory predictions to generate motor commands to attain a sensory goal.

Sensorimotor control point

A planned contact event in which predicted and actual sensory signals are compared to assess the outcome of an executed action-phase controller.

Transcranial magnetic stimulation

(TMS). A non-invasive technique that can be used to induce a transient interruption of normal activity in a restricted area of the brain. It is based on the generation of a magnetic pulse near the area of interest that induces small eddy currents that stimulate neurons.

Grasp stability

The control of grip forces such that they are adequate to prevent accidental slips but not so large that they cause unnecessary fatigue or damage to the object or hand.

Forward internal models

Neural circuits that mimic the behaviour of the motor system and environment and capture the mapping between motor commands and expected sensory consequences.

Corollary discharge

An internal signal, derived in part from motor commands, that can be used to estimate the time-varying afferent input that corresponds to the predicted sensory consequences of the motor command.

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Johansson, R., Flanagan, J. Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10, 345–359 (2009). https://doi.org/10.1038/nrn2621

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