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Journal Articles Communications Biology Year : 2023

Neuroprosthetics: from sensorimotor to cognitive disorders

Ankur Gupta
  • Function : Author
Nikolaos Vardalakis

Abstract

Neuroprosthetics is a multidisciplinary field at the interface between neurosciences and biomedical engineering, which aims at replacing or modulating parts of the nervous system that get disrupted in neurological disorders or after injury. Although neuroprostheses have steadily evolved over the past 60 years in the field of sensory and motor disorders, their application to higher-order cognitive functions is still at a relatively preliminary stage. Nevertheless, a recent series of proof-of-concept studies suggest that electrical neuromodulation strategies might also be useful in alleviating some cognitive and memory deficits, in particular in the context of dementia. Here, we review the evolution of neuroprosthetics from sensorimotor to cognitive disorders, highlighting important common principles such as the need for neuroprosthetic systems that enable multisite bidirectional interactions with the nervous system. N eural oscillations are ubiquitous throughout the nervous system, subserving sensory, motor, and cognitive functions in the brain and the spinal cord 1. These oscillations are often disrupted in neurodegenerative and neuropsychiatric disorders 2 , after stroke 3 , traumatic brain injury 4 , or spinal cord injury (SCI) 5. Despite different underlying mechanisms, abnormal or even abolished neural oscillations seem to be a hallmark of neurological disorders and to play a causative role in their behavioral symptoms 6. In recent years, bioelectronic devices that interface with the nervous system and affect or reestablish these oscillations have become an alternative to pharmacological treatments, opening a new era of medicine consisting of electroceuticals, Brain-Computer or Brain-Machine Interfaces (BCI/BMI), and neuroprostheses 7-10. These bioelectronic devices can now treat some motor symptoms of Parkinson's disease (PD) 11 or restore motor function after SCI 12-14. However, cognitive disorders still elude this new therapeutic modality, due to the intrinsic complexity of the neural mechanisms underlying cognition and to technological challenges for modulating the associated networks. Whether they result from brain injury or neurodegenerative diseases such as Alzheimer's disease (AD), cognitive disorders do not yet have efficient pharmacological treatments, represent a major public health issue, and could potentially benefit from neuromodulation strategies 15. Here, we review the current state of the art on neuromodulation and neuroprosthetic approaches for sensorimotor and cognitive disorders, with a focus on invasive neurotechnologies tested in non-human primates (NHP) and humans. We first introduce the concept of motor neuroprostheses for motor impairments resulting from stroke or SCI, and somatosensory neuroprostheses for providing sensory feedback after limb amputation or paralysis. Next, we present deep brain stimulation (DBS) for motor and cognitive symptoms of PD. We then discuss the neural oscillations that characterize cognitive functions, especially learning and memory, and their alterations in memory disorders. This is followed by a state of the art on neuromodulation approaches for AD and other memory impairments. Finally, we present the enticing hypothesis that cognitive deficits would particularly benefit from the development of a new generation of neuroprosthetic systems that target large-scale brain network oscillations and facilitate the associated neurological functions.
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Dates and versions

hal-03947149 , version 1 (19-01-2023)

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Ankur Gupta, Nikolaos Vardalakis, Fabien Bertrand Paul Wagner. Neuroprosthetics: from sensorimotor to cognitive disorders. Communications Biology, 2023, 6, ⟨10.1038/s42003-022-04390-w⟩. ⟨hal-03947149⟩

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