Long-Term Sheep Implantation of WIMAGINE®, a Wireless 64-Channel Electrocorticogram Recorder

This article deals with the long-term preclinical validation of WIMAGINE® (Wireless Implantable Multi-channel Acquisition system for Generic Interface with Neurons), a 64-channel wireless implantable recorder that measures the electrical activity at the cortical surface (electrocorticography, ECoG). The WIMAGINE® implant was designed for chronic wireless neuronal signal acquisition, to be used e.g., as an intracranial Brain–Computer Interface (BCI) for severely motor-impaired patients. Due to the size and shape of WIMAGINE®, sheep appeared to be the best animal model on which to carry out long-term in vivo validation. The devices were implanted in two sheep for a follow-up period of 10 months, including idle state cortical recordings and Somato-Sensory Evoked Potential (SSEP) sessions. ECoG and SSEP demonstrated relatively stable behavior during the 10-month observation period. Information recorded from the SensoriMotor Cortex (SMC) showed an SSEP phase reversal, indicating the cortical site of the sensorimotor activity was retained after 10 months of contact. Based on weekly recordings of raw ECoG signals, the effective bandwidth was in the range of 230 Hz for both animals and remarkably stable over time, meaning preservation of the high frequency bands valuable for decoding of the brain activity using BCIs. The power spectral density (in dB/Hz), on a log scale, was of the order of 2.2, –4.5 and –18 for the frequency bands (10–40), (40–100), and (100–200) Hz, respectively. The outcome of this preclinical work is the first long-term in vivo validation of the WIMAGINE® implant, highlighting its ability to record the brain electrical activity through the dura mater and to send wireless digitized data to the external base station. Apart from local adhesion of the dura to the skull, the neurosurgeon did not face any difficulty in the implantation of the WIMAGINE® device and post-mortem analysis of the brain revealed no side effect related to the implantation. We also report on the reliability of the system; including the implantable device, the antennas module and the external base station.

[1]  Leonid Churilov,et al.  Minimally invasive endovascular stent-electrode array for high-fidelity, chronic recordings of cortical neural activity , 2016, Nature Biotechnology.

[2]  Pedram Afshar,et al.  Chronic cortical and electromyographic recordings from a fully implantable device: preclinical experience in a nonhuman primate , 2014, Journal of neural engineering.

[3]  Guillaume Charvet,et al.  A Low-Power 0.7 $\mu {\rm V_{rms}}$ 32-Channel Mixed-Signal Circuit for ECoG Recordings , 2011, IEEE Journal on Emerging and Selected Topics in Circuits and Systems.

[4]  David B. Grayden,et al.  Consistency of Long-Term Subdural Electrocorticography in Humans , 2017, IEEE Transactions on Biomedical Engineering.

[5]  Nicholas P. Szrama,et al.  Characterization of the effects of the human dura on macro- and micro-electrocorticographic recordings , 2014, Journal of neural engineering.

[6]  Guillaume Charvet,et al.  WIMAGINE: Wireless 64-Channel ECoG Recording Implant for Long Term Clinical Applications , 2015, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[7]  Nicholas P. Szrama,et al.  Histological evaluation of a chronically-implanted electrocorticographic electrode grid in a non-human primate , 2016, Journal of neural engineering.

[8]  P. Gerszten,et al.  Safety and efficacy of a novel ultrasonic osteotome device in an ovine model , 2011, Journal of Clinical Neuroscience.

[9]  N. Ramsey,et al.  Fully Implanted Brain-Computer Interface in a Locked-In Patient with ALS. , 2016, The New England journal of medicine.

[10]  Bin He,et al.  Imaging epileptogenic brain using high density EEG source imaging and MRI , 2016, Clinical Neurophysiology.

[11]  A. Benabid,et al.  Neuroprotective Surgical Strategies in Parkinson’s Disease: Role of Preclinical Data , 2017, International journal of molecular sciences.

[12]  Tonio Ball,et al.  Closed-loop interaction with the cerebral cortex: a review of wireless implant technology§ , 2017 .

[13]  Tonio Ball,et al.  Evaluation of μECoG electrode arrays in the minipig: Experimental procedure and neurosurgical approach , 2011, Journal of Neuroscience Methods.

[14]  Tibor Ujbanyi,et al.  Speed control of Festo Robotino mobile robot using NeuroSky MindWave EEG headset based brain-computer interface , 2016, 2016 7th IEEE International Conference on Cognitive Infocommunications (CogInfoCom).

[15]  P. Brown,et al.  Beta burst coupling across the motor circuit in Parkinson's disease , 2018, Neurobiology of Disease.

[16]  A. Michael,et al.  Brain Tissue Responses to Neural Implants Impact Signal Sensitivity and Intervention Strategies , 2014, ACS chemical neuroscience.

[17]  Andrey Eliseyev,et al.  Recursive N-Way Partial Least Squares for Brain-Computer Interface , 2013, PloS one.

[18]  A. Krieger,et al.  Intracranial EEG fluctuates over months after implanting electrodes in human brain , 2017, Journal of neural engineering.

[19]  P. Maciejasz,et al.  Selective ENG recordings using a multi-contact cuff electrode , 2013, 2013 6th International IEEE/EMBS Conference on Neural Engineering (NER).

[20]  I. Whittle,et al.  Effect of halothane on spinal somatosensory evoked potentials in sheep. , 1985, British journal of anaesthesia.

[21]  Ramin Pashaie,et al.  The effect of micro-ECoG substrate footprint on the meningeal tissue response , 2014, Journal of neural engineering.

[22]  Andrew B. Schwartz,et al.  Brain-Controlled Interfaces: Movement Restoration with Neural Prosthetics , 2006, Neuron.

[23]  R A Normann,et al.  The Utah intracortical Electrode Array: a recording structure for potential brain-computer interfaces. , 1997, Electroencephalography and clinical neurophysiology.

[24]  Naotaka Fujii,et al.  Long-Term Asynchronous Decoding of Arm Motion Using Electrocorticographic Signals in Monkeys , 2009, Front. Neuroeng..

[25]  David M. Himes,et al.  Prediction of seizure likelihood with a long-term, implanted seizure advisory system in patients with drug-resistant epilepsy: a first-in-man study , 2013, The Lancet Neurology.

[26]  Tonio Ball,et al.  Mapping of sheep sensory cortex with a novel microelectrocorticography grid , 2014, The Journal of comparative neurology.

[27]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[28]  Greg Worrell,et al.  Long-Term Measurement of Impedance in Chronically Implanted Depth and Subdural Electrodes During Responsive Neurostimulation in Humans , 2013, Brain Stimulation.

[29]  Svjetlana Miocinovic,et al.  Chronic multisite brain recordings from a totally implantable bidirectional neural interface: experience in 5 patients with Parkinson's disease. , 2017, Journal of neurosurgery.

[30]  Robin C. Ashmore,et al.  An Electrocorticographic Brain Interface in an Individual with Tetraplegia , 2013, PloS one.

[31]  R. Normann,et al.  Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex , 1998, Journal of Neuroscience Methods.