Restoring Somatosensation: Advantages and Current Limitations of Targeting the Brainstem Dorsal Column Nuclei Complex

Abstract

Current neural prostheses can restore limb movement to tetraplegic patients by translating brain signals coding movements to control a variety of actuators. Fast and accurate somatosensory feedback is essential for normal movement, particularly dexterous tasks, but is currently lacking in motor neural prostheses. Attempts to restore somatosensory feedback have largely focused on cortical stimulation which, thus far, have succeeded in eliciting minimal naturalistic sensations. Yet, a question that deserves more attention is whether the cortex is the best place to activate the central nervous system to restore somatosensation. Here, we propose that the brainstem dorsal column nuclei are an ideal alternative target to restore somatosensation. We review some of the recent literature investigating the dorsal column nuclei functional organization and neurophysiology and highlight some of the advantages and limitations of the dorsal column nuclei as a future neural prosthetic target. Recent evidence supports the dorsal column nuclei as a potential neural prosthetic target, but also identifies several gaps in our knowledge as well as potential limitations which need to be addressed before such a goal can become reality.

Tapping Into the Language of Touch: Using Non-invasive Stimulation to Specify Tactile Afferent Firing Patterns

“…This aggregation would occur at the first central nervous system synapse, which for the main tactile pathways are in the dorsal column nuclei. These nuclei are also a focus for a possible brainmachine interface, with early work showing potential for decoding the afferent input signals using machine-learning techniques (Sritharan et al, 2016;Loutit et al, 2017Loutit et al, , 2019Loutit and Potas, 2020).…”

Functional Organisation and Connectivity of the Dorsal Column Nuclei Complex Reveals a Sensorimotor Integration and Distribution Hub

“…Understanding sensorimotor functions of the brain, of which reaching and grasping functions are of the highest importance, is a central question in neuroscience. The DCN has recently received attention for its potential for restoring somatosensory function (Loutit & Potas, 2020). Here, we review the morphology, organisation, and afferent and efferent connections of the DCN and associated nuclei, with discussion of functional implications.…”

Dorsal Column Nuclei Neural Signal Features Permit Robust Machine-Learning of Natural Tactile- and Proprioception-Dominated Stimuli

“…Several groups have stimulated monkey or human somatosensory cortex to evoke percepts such as vibration, pressure, and stimulus location, and have shown that this somatosensory feedback improves dexterous manipulation capabilities of motor neural prostheses (O’Doherty et al, 2009 , 2019 ; Tabot et al, 2013 ; Klaes et al, 2014 ; Kim et al, 2015 ; Flesher et al, 2016 , 2019 ; Salas et al, 2018 ). However, we have recently suggested that the dorsal column nuclei (DCN) and their associated external cuneate nuclei, nuclei X, and Z (DCN-complex) have anatomical advantages over the cortex as a sensory neural prosthesis target (Loutit and Potas, 2020a ; Loutit et al, 2020 ). Activating the DCN-complex with a neural prosthesis capable of mimicking natural somatosensory signals has the potential to simultaneously inform not only the cortex but several other regions essential for motor control, including the cerebellum and tegmentum that are bypassed by a cortical neural prosthesis.…”

“…While the DCN has begun to receive attention as a neural prosthetic target, microelectrode arrays have been chronically implanted in macaque DCN (Richardson et al, 2015 ; Sritharan et al, 2016 ; Loutit et al, 2017 , 2019 ; Suresh et al, 2017 ; Loutit and Potas, 2020a ). To date, these DCN rigid chronic electrode array implants have resulted in some failures due to head and neck movements damaging the wire bundles or dislodging the array from the brain tissue (Suresh et al, 2017 ).…”

“…To date, these DCN rigid chronic electrode array implants have resulted in some failures due to head and neck movements damaging the wire bundles or dislodging the array from the brain tissue (Suresh et al, 2017 ). However, rapidly advancing soft implantable electrode technologies, such as microelectrode “threads” that can be sewn into brain tissue at densities of approximately 3,000 electrodes/25 mm 2 (Musk and Neuralink, 2019 ), present a promising solution for targeting the DCN (Loutit and Potas, 2020a ). Yet, knowledge of DCN neurophysiology and how to effectively activate DCN neural populations to restore somatosensory feedback is limited.…”