Phantom Limbs, Neuroprosthetics, and the Developmental Origins of Embodiment

Abstract

Amputees who wish to rid themselves of a phantom limb must weaken the neural representation of the absent limb. Conversely, amputees who wish to replace a lost limb must assimilate a neuroprosthetic with the existing neural representation. Whether we wish to remove a phantom limb or assimilate a synthetic one, we will benefit from knowing more about the developmental process that enables embodiment. A potentially critical contributor to that process is the spontaneous activity - in the form of limb twitches - that occurs exclusively and abundantly during active (REM) sleep, a particularly prominent state in early development. The sensorimotor circuits activated by twitching limbs, and the developmental context in which activation occurs, could provide a roadmap for creating neuroprosthetics that feel as if they are part of the body.

Keywords: REM sleep; body schema; brain–machine interface; cerebellum; development; motor cortex; myoclonic twitching; neural circuit.

Figure 1

Twitches are Produced Discretely and are Spatiotemporally Organized. (A) Sequential high-speed video frames in an 8-day-old rat to show the discrete nature of twitching, illustrated here using the left elbow (top) and right shoulder (bottom). The yellow arrows indicate the direction in which the limb is moving and the white markers were used for motion tracking of limb movements. (B) Records of limb twitching in an 8-day-old rat at a long (top) and short (bottom) timescale to illustrate the discreteness and spatiotemporal organization of twitching; the segment denoted by the gray box is expanded below. Each tick mark indicates a single twitch at the shoulder, elbow, or wrist in the right (red) or left (blue) forelimb. Solid and dashed lines indicate the direction of movement at each joint (i.e., flexion or extension, adduction or abduction). Adapted from [16].

Figure 2

Circuit Diagram Illustrating the Web of Neural Structures that Support Embodiment. (A) Some major sensorimotor structures involved in the production of movement and the processing of reafferent signals. Reafference from twitching limbs triggers neural activity within all of the sensorimotor loops shown: These loops include afferent and efferent projections from nuclei in the mesodiencephalic junction (MDJ; red), cerebellum (blue), and sensorimotor cortex (green). Importantly, the limb receives motor commands from both motor cortex and nuclei in the MDJ (including the red nucleus), and the reafferent pathways complete each loop, allowing each structure to monitor and update its representation of the limb. IO, inferior olive; LRN, lateral reticular nucleus. (B) A phantom limb is perceived when the limb is absent, but the sensorimotor structures representing the limb remain intact. Without reafference to update the limb’s neural representation, the phantom limb persists. (C) A closed-loop neuroprosthetic limb interfaces directly with motor cortex and sensory cortex (yellow arrows), providing reafference that bypasses subcortical sensorimotor structures. By interacting exclusively or primarily with sensorimotor cortex, the rest of the existing limb representation is unaltered, thereby limiting the incorporation of the neuroprosthetic limb into the body schema.