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NeuroGrid: recording action potentials from the surface of the brain.

Khodagholy D, Gelinas JN, Thesen T, Doyle W, Devinsky O, Malliaras GG, Buzsáki G - Nat. Neurosci. (2014)

Bottom Line: Here, we address this challenge by developing an organic material-based, ultraconformable, biocompatible and scalable neural interface array (the 'NeuroGrid') that can record both local field potentials(LFPs) and action potentials from superficial cortical neurons without penetrating the brain surface.We also recorded LFP-modulated spiking activity intraoperatively in patients undergoing epilepsy surgery.The NeuroGrid constitutes an effective method for large-scale, stable recording of neuronal spikes in concert with local population synaptic activity, enhancing comprehension of neural processes across spatiotemporal scales and potentially facilitating diagnosis and therapy for brain disorders.

View Article: PubMed Central - PubMed

Affiliation: NYU Neuroscience Institute, School of Medicine, New York University, New York, New York, USA.

ABSTRACT
Recording from neural networks at the resolution of action potentials is critical for understanding how information is processed in the brain. Here, we address this challenge by developing an organic material-based, ultraconformable, biocompatible and scalable neural interface array (the 'NeuroGrid') that can record both local field potentials(LFPs) and action potentials from superficial cortical neurons without penetrating the brain surface. Spikes with features of interneurons and pyramidal cells were simultaneously acquired by multiple neighboring electrodes of the NeuroGrid, allowing for the isolation of putative single neurons in rats. Spiking activity demonstrated consistent phase modulation by ongoing brain oscillations and was stable in recordings exceeding 1 week's duration. We also recorded LFP-modulated spiking activity intraoperatively in patients undergoing epilepsy surgery. The NeuroGrid constitutes an effective method for large-scale, stable recording of neuronal spikes in concert with local population synaptic activity, enhancing comprehension of neural processes across spatiotemporal scales and potentially facilitating diagnosis and therapy for brain disorders.

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NeuroGrid structure and spike recordings in freely moving rats.a) The NeuroGrid conforms to the surface of an orchid petal (scale = 5mm). Optical micrograph (inset) of a 256 electrode NeuroGrid (scale = 100 μm). Electrodes are 10 × 10 μm2 with 30 μm inter-electrode spacing.b) The NeuroGrid conforms to the surface of rat somatosensory cortex. The edge of the resected dura is visible in the top left corner of the craniotomy (scale = 1 mm).c) High-pass filtered (fc = 500Hz) time traces recorded in a freely moving rat from the surface of cortex (left) and hippocampus (right) in black. Corresponding postmortem filtered traces (rms noise = 3 μV at spike bandwidth) are in red (scale = 10 ms by 50 μV).d) Examples of the spatial extent of extracellular action potentials in cortex (left) and hippocampus (right) over the geometry of the NeuroGrid by spike-triggered averaging during the detected spike times (scale = 1.5 ms by 50 μV).e) Mean and standard deviation of the amplitude of detected action potential waveforms across 10 days of recording. The average amplitude and the variability of hippocampal waveforms (blue) are larger than cortical waveforms (black). The red curve demonstrates the spike detection threshold (rms noise = 8 μV at 0.1 – 7500 Hz).
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Figure 1: NeuroGrid structure and spike recordings in freely moving rats.a) The NeuroGrid conforms to the surface of an orchid petal (scale = 5mm). Optical micrograph (inset) of a 256 electrode NeuroGrid (scale = 100 μm). Electrodes are 10 × 10 μm2 with 30 μm inter-electrode spacing.b) The NeuroGrid conforms to the surface of rat somatosensory cortex. The edge of the resected dura is visible in the top left corner of the craniotomy (scale = 1 mm).c) High-pass filtered (fc = 500Hz) time traces recorded in a freely moving rat from the surface of cortex (left) and hippocampus (right) in black. Corresponding postmortem filtered traces (rms noise = 3 μV at spike bandwidth) are in red (scale = 10 ms by 50 μV).d) Examples of the spatial extent of extracellular action potentials in cortex (left) and hippocampus (right) over the geometry of the NeuroGrid by spike-triggered averaging during the detected spike times (scale = 1.5 ms by 50 μV).e) Mean and standard deviation of the amplitude of detected action potential waveforms across 10 days of recording. The average amplitude and the variability of hippocampal waveforms (blue) are larger than cortical waveforms (black). The red curve demonstrates the spike detection threshold (rms noise = 8 μV at 0.1 – 7500 Hz).

Mentions: We recorded action potentials from the surface of the neocortex and hippocampus with the NeuroGrid. We have determined that the ability of the array to isolate single neuron action potentials is a product of several design elements: (i) recording electrode density that matches the average size of neuronal bodies and neuronal density (10 × 10 μm2 electrode surface area and 30 μm inter-electrode spacing; Fig. 1a inset and Supplementary Fig. 1a); (ii) use of poly (3,4-ethylenedioxythiophene) doped with poly(styrenesulfonate) (PEDOT:PSS) as the interface material, which significantly decreases electrochemical impedance mismatch between tissue and electrodes due to its mixed electronic/ionic conductivity and high ionic mobility15,16 (Supplementary Fig. 1d); (iii) encapsulation with parylene C, to allow microfabrication of a thin (4 μm) and ultra-conformable structure that can closely adhere to complex curvilinear surfaces (Fig. 1a and Supplementary Fig. 1b). The entire microfabrication process was based on generic photolithographic patterning17,18. Pt and Au, used as interconnects and pads, were embedded at the mechanical neutral plane of the device (2 μm depth) to generate a robust mechanical structure able to conform to a small bending radius (Supplementary Fig. 1b). These metallic structures were completely covered with PEDOT:PSS or parylene C to prevent any exposure to brain tissue. Au was used as an inert substrate for PEDOT:PSS deposition coupled with Pt as a bonding pad, thereby eliminating the need for bulky connectors between the PEDOT:PSS-based flexible electrodes and conventional rigid electronic components. These design elements result in low levels of noise, high stability of electrode response over time and improved signal-to-noise ratio (Supplementary Figs. 1c-d and 2).


NeuroGrid: recording action potentials from the surface of the brain.

Khodagholy D, Gelinas JN, Thesen T, Doyle W, Devinsky O, Malliaras GG, Buzsáki G - Nat. Neurosci. (2014)

NeuroGrid structure and spike recordings in freely moving rats.a) The NeuroGrid conforms to the surface of an orchid petal (scale = 5mm). Optical micrograph (inset) of a 256 electrode NeuroGrid (scale = 100 μm). Electrodes are 10 × 10 μm2 with 30 μm inter-electrode spacing.b) The NeuroGrid conforms to the surface of rat somatosensory cortex. The edge of the resected dura is visible in the top left corner of the craniotomy (scale = 1 mm).c) High-pass filtered (fc = 500Hz) time traces recorded in a freely moving rat from the surface of cortex (left) and hippocampus (right) in black. Corresponding postmortem filtered traces (rms noise = 3 μV at spike bandwidth) are in red (scale = 10 ms by 50 μV).d) Examples of the spatial extent of extracellular action potentials in cortex (left) and hippocampus (right) over the geometry of the NeuroGrid by spike-triggered averaging during the detected spike times (scale = 1.5 ms by 50 μV).e) Mean and standard deviation of the amplitude of detected action potential waveforms across 10 days of recording. The average amplitude and the variability of hippocampal waveforms (blue) are larger than cortical waveforms (black). The red curve demonstrates the spike detection threshold (rms noise = 8 μV at 0.1 – 7500 Hz).
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Figure 1: NeuroGrid structure and spike recordings in freely moving rats.a) The NeuroGrid conforms to the surface of an orchid petal (scale = 5mm). Optical micrograph (inset) of a 256 electrode NeuroGrid (scale = 100 μm). Electrodes are 10 × 10 μm2 with 30 μm inter-electrode spacing.b) The NeuroGrid conforms to the surface of rat somatosensory cortex. The edge of the resected dura is visible in the top left corner of the craniotomy (scale = 1 mm).c) High-pass filtered (fc = 500Hz) time traces recorded in a freely moving rat from the surface of cortex (left) and hippocampus (right) in black. Corresponding postmortem filtered traces (rms noise = 3 μV at spike bandwidth) are in red (scale = 10 ms by 50 μV).d) Examples of the spatial extent of extracellular action potentials in cortex (left) and hippocampus (right) over the geometry of the NeuroGrid by spike-triggered averaging during the detected spike times (scale = 1.5 ms by 50 μV).e) Mean and standard deviation of the amplitude of detected action potential waveforms across 10 days of recording. The average amplitude and the variability of hippocampal waveforms (blue) are larger than cortical waveforms (black). The red curve demonstrates the spike detection threshold (rms noise = 8 μV at 0.1 – 7500 Hz).
Mentions: We recorded action potentials from the surface of the neocortex and hippocampus with the NeuroGrid. We have determined that the ability of the array to isolate single neuron action potentials is a product of several design elements: (i) recording electrode density that matches the average size of neuronal bodies and neuronal density (10 × 10 μm2 electrode surface area and 30 μm inter-electrode spacing; Fig. 1a inset and Supplementary Fig. 1a); (ii) use of poly (3,4-ethylenedioxythiophene) doped with poly(styrenesulfonate) (PEDOT:PSS) as the interface material, which significantly decreases electrochemical impedance mismatch between tissue and electrodes due to its mixed electronic/ionic conductivity and high ionic mobility15,16 (Supplementary Fig. 1d); (iii) encapsulation with parylene C, to allow microfabrication of a thin (4 μm) and ultra-conformable structure that can closely adhere to complex curvilinear surfaces (Fig. 1a and Supplementary Fig. 1b). The entire microfabrication process was based on generic photolithographic patterning17,18. Pt and Au, used as interconnects and pads, were embedded at the mechanical neutral plane of the device (2 μm depth) to generate a robust mechanical structure able to conform to a small bending radius (Supplementary Fig. 1b). These metallic structures were completely covered with PEDOT:PSS or parylene C to prevent any exposure to brain tissue. Au was used as an inert substrate for PEDOT:PSS deposition coupled with Pt as a bonding pad, thereby eliminating the need for bulky connectors between the PEDOT:PSS-based flexible electrodes and conventional rigid electronic components. These design elements result in low levels of noise, high stability of electrode response over time and improved signal-to-noise ratio (Supplementary Figs. 1c-d and 2).

Bottom Line: Here, we address this challenge by developing an organic material-based, ultraconformable, biocompatible and scalable neural interface array (the 'NeuroGrid') that can record both local field potentials(LFPs) and action potentials from superficial cortical neurons without penetrating the brain surface.We also recorded LFP-modulated spiking activity intraoperatively in patients undergoing epilepsy surgery.The NeuroGrid constitutes an effective method for large-scale, stable recording of neuronal spikes in concert with local population synaptic activity, enhancing comprehension of neural processes across spatiotemporal scales and potentially facilitating diagnosis and therapy for brain disorders.

View Article: PubMed Central - PubMed

Affiliation: NYU Neuroscience Institute, School of Medicine, New York University, New York, New York, USA.

ABSTRACT
Recording from neural networks at the resolution of action potentials is critical for understanding how information is processed in the brain. Here, we address this challenge by developing an organic material-based, ultraconformable, biocompatible and scalable neural interface array (the 'NeuroGrid') that can record both local field potentials(LFPs) and action potentials from superficial cortical neurons without penetrating the brain surface. Spikes with features of interneurons and pyramidal cells were simultaneously acquired by multiple neighboring electrodes of the NeuroGrid, allowing for the isolation of putative single neurons in rats. Spiking activity demonstrated consistent phase modulation by ongoing brain oscillations and was stable in recordings exceeding 1 week's duration. We also recorded LFP-modulated spiking activity intraoperatively in patients undergoing epilepsy surgery. The NeuroGrid constitutes an effective method for large-scale, stable recording of neuronal spikes in concert with local population synaptic activity, enhancing comprehension of neural processes across spatiotemporal scales and potentially facilitating diagnosis and therapy for brain disorders.

Show MeSH
Related in: MedlinePlus