Restoring tactile and proprioceptive sensation through a brain interface

Abstract

Somatosensation plays a critical role in the dexterous manipulation of objects, in emotional communication, and in the embodiment of our limbs. For upper-limb neuroprostheses to be adopted by prospective users, prosthetic limbs will thus need to provide sensory information about the position of the limb in space and about objects grasped in the hand. One approach to restoring touch and proprioception consists of electrically stimulating neurons in somatosensory cortex in the hopes of eliciting meaningful sensations to support the dexterous use of the hands, promote their embodiment, and perhaps even restore the affective dimension of touch. In this review, we discuss the importance of touch and proprioception in everyday life, then describe approaches to providing artificial somatosensory feedback through intracortical microstimulation (ICMS). We explore the importance of biomimicry--the elicitation of naturalistic patterns of neuronal activation--and that of adaptation--the brain's ability to adapt to novel sensory input, and argue that both biomimicry and adaptation will play a critical role in the artificial restoration of somatosensation. We also propose that the documented re-organization that occurs after injury does not pose a significant obstacle to brain interfaces. While still at an early stage of development, sensory restoration is a critical step in transitioning upper-limb neuroprostheses from the laboratory to the clinic.

Keywords: Brain–machine interface; Intracortical microstimulation; Neuroprosthetics; Somatosensation; Somatosensory cortex.

Figure 1. Primary somatosensory cortex

a. Primary somatosensory cortex is located in anterior parietal cortex, on the post-central gyrus, and comprises four modules, Brodmann’s areas 3a, 3b, 1 and 2. Neurons in area 3a respond primarily to joint movements, neurons in areas 3b and 1 respond to cutaneous stimulation, and neurons in area 2 exhibit both proprioceptive and cutaneous responses. b. Orientation-selective neuron in area 3b: This neuron responds preferentially when an edge whose orientation is parallel to the long axis of the digit is indented into the fingertip (Bensmaia et al., 2008). c. Direction-selective (cutaneous) neuron in area 1: This neuron responds preferentially when a stimulus (in this case an edge) is scanned across the fingertip in the distal-to-proximal direction (Pei et al., 2010). d. Direction-selective (proprioceptive) neuron in area 2: This neuron responds preferentially to a limb deflection in the proximal-to-distal direction (towards the body)(London and Miller, 2013).

Figure 2. Biomimetic approach

a. Contact location: Stimulating a local population of S1 neurons elicits a percept that is projected to the receptive field of those neurons on the skin. b. Contact pressure: Pressure signals from the sensors on the hand can be converted into electrical pulse trains that elicit sensations of appropriate sensory magnitude. c. Timing of contact events: The top trace shows the temporal profile of two indentations into the skin. The middle trace, a representation of the evoked response, and the bottom trace the biomimetic pulse train that signals contact. With an intact arm and nervous system, contact events are signaled by strong transient responses in almost all S1 neurons. These transients can be replicated by delivering phasic pulse trains triggered at the onset and offset of contact. Note that, a force-related signal (not shown) would be superimposed on the contact-related one.

Figure 3. Example of the adaptation approach

The direction and speed of a random dot stereogram indicate to the animal the relative location and distance of the target, respectively. The patterning in and strength of ICMS convey redundant information about the relative location and distance of the target, respectively. The animal is trained with visual stimulation and ICMS but eventually can do the task based on artificial feedback alone (Dadarlat et al., 2012).