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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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Intra-operative NeuroGrid recording of LFP and spikes in epilepsy patients.a) Surgical placement of the NeuroGrid on the surface of human brain (open circle). Acquisition electronics are suspended above the cortical surface. Two stainless steel needle electrodes served as ground and reference electrodes adjacent to the craniotomy (scale = 2 cm).b) High-pass filtered (fc = 250 Hz) time traces of the intra-operative NeuroGrid recordings containing spiking activity (scale = 20 ms by 40 μV). Sample spike waveforms obtained by spike-triggered averaging of spikes from different recording sites (scale = 1 ms, 40 μV).c) Sample time-frequency spectrogram of intra-operative recordings under anesthesia from an epilepsy patient (scale = 500 ms by 500 μV).d) Sample multi-channel LFP recording during intra-operative anesthesia (black traces) overlaid on time-frequency spectrogram filtered at beta frequency (18 – 25 Hz). Areas with high beta frequency power are located in spatially coherent clusters on the NeuroGrid (inset; scale = 500 ms, 750 μV).e) Polar plot and histogram demonstrating decreased spike firing during the trough of the slow oscillation. Black lines superimposed on the histogram correspond to phase modulation of spikes on different channels.
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Figure 4: Intra-operative NeuroGrid recording of LFP and spikes in epilepsy patients.a) Surgical placement of the NeuroGrid on the surface of human brain (open circle). Acquisition electronics are suspended above the cortical surface. Two stainless steel needle electrodes served as ground and reference electrodes adjacent to the craniotomy (scale = 2 cm).b) High-pass filtered (fc = 250 Hz) time traces of the intra-operative NeuroGrid recordings containing spiking activity (scale = 20 ms by 40 μV). Sample spike waveforms obtained by spike-triggered averaging of spikes from different recording sites (scale = 1 ms, 40 μV).c) Sample time-frequency spectrogram of intra-operative recordings under anesthesia from an epilepsy patient (scale = 500 ms by 500 μV).d) Sample multi-channel LFP recording during intra-operative anesthesia (black traces) overlaid on time-frequency spectrogram filtered at beta frequency (18 – 25 Hz). Areas with high beta frequency power are located in spatially coherent clusters on the NeuroGrid (inset; scale = 500 ms, 750 μV).e) Polar plot and histogram demonstrating decreased spike firing during the trough of the slow oscillation. Black lines superimposed on the histogram correspond to phase modulation of spikes on different channels.

Mentions: After establishing the recording ability of the NeuroGrid in rats, we performed intra-operative recordings over mid-superior temporal gyrus in two patients undergoing epilepsy surgery. The NeuroGrid was placed on the pial surface after removal of the chronic diagnostic subdural grid in one patient, and after intra-operative clinical ECoG and tumor resection in the other patient (Fig. 4a). Due to its conformability and hydrophobic surface (parylene C), the NeuroGrid made stable electrical and mechanical contact with the cortical surface despite brain pulsations. Cortical slow oscillations interspersed with higher frequency activity were observed (Fig. 4c–d), commensurate with surgical anesthesia. Beta-frequency oscillations exhibited differential power across channels and formed spatially coherent clusters of activity (Fig. 4d). High-pass filtered traces revealed spiking activity (Fig. 4b). Although the limited intra-operative recording time (8 and 20 min) and the lower amplitude spikes compared to recording in rodents precluded reliable clustering of putative single neurons, spikes displayed typical waveform patterns (Fig. 4b) and were reliably phase-modulated by cortical slow oscillations (Fig. 4e), confirming the physiologic nature of the activity.


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)

Intra-operative NeuroGrid recording of LFP and spikes in epilepsy patients.a) Surgical placement of the NeuroGrid on the surface of human brain (open circle). Acquisition electronics are suspended above the cortical surface. Two stainless steel needle electrodes served as ground and reference electrodes adjacent to the craniotomy (scale = 2 cm).b) High-pass filtered (fc = 250 Hz) time traces of the intra-operative NeuroGrid recordings containing spiking activity (scale = 20 ms by 40 μV). Sample spike waveforms obtained by spike-triggered averaging of spikes from different recording sites (scale = 1 ms, 40 μV).c) Sample time-frequency spectrogram of intra-operative recordings under anesthesia from an epilepsy patient (scale = 500 ms by 500 μV).d) Sample multi-channel LFP recording during intra-operative anesthesia (black traces) overlaid on time-frequency spectrogram filtered at beta frequency (18 – 25 Hz). Areas with high beta frequency power are located in spatially coherent clusters on the NeuroGrid (inset; scale = 500 ms, 750 μV).e) Polar plot and histogram demonstrating decreased spike firing during the trough of the slow oscillation. Black lines superimposed on the histogram correspond to phase modulation of spikes on different channels.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4308485&req=5

Figure 4: Intra-operative NeuroGrid recording of LFP and spikes in epilepsy patients.a) Surgical placement of the NeuroGrid on the surface of human brain (open circle). Acquisition electronics are suspended above the cortical surface. Two stainless steel needle electrodes served as ground and reference electrodes adjacent to the craniotomy (scale = 2 cm).b) High-pass filtered (fc = 250 Hz) time traces of the intra-operative NeuroGrid recordings containing spiking activity (scale = 20 ms by 40 μV). Sample spike waveforms obtained by spike-triggered averaging of spikes from different recording sites (scale = 1 ms, 40 μV).c) Sample time-frequency spectrogram of intra-operative recordings under anesthesia from an epilepsy patient (scale = 500 ms by 500 μV).d) Sample multi-channel LFP recording during intra-operative anesthesia (black traces) overlaid on time-frequency spectrogram filtered at beta frequency (18 – 25 Hz). Areas with high beta frequency power are located in spatially coherent clusters on the NeuroGrid (inset; scale = 500 ms, 750 μV).e) Polar plot and histogram demonstrating decreased spike firing during the trough of the slow oscillation. Black lines superimposed on the histogram correspond to phase modulation of spikes on different channels.
Mentions: After establishing the recording ability of the NeuroGrid in rats, we performed intra-operative recordings over mid-superior temporal gyrus in two patients undergoing epilepsy surgery. The NeuroGrid was placed on the pial surface after removal of the chronic diagnostic subdural grid in one patient, and after intra-operative clinical ECoG and tumor resection in the other patient (Fig. 4a). Due to its conformability and hydrophobic surface (parylene C), the NeuroGrid made stable electrical and mechanical contact with the cortical surface despite brain pulsations. Cortical slow oscillations interspersed with higher frequency activity were observed (Fig. 4c–d), commensurate with surgical anesthesia. Beta-frequency oscillations exhibited differential power across channels and formed spatially coherent clusters of activity (Fig. 4d). High-pass filtered traces revealed spiking activity (Fig. 4b). Although the limited intra-operative recording time (8 and 20 min) and the lower amplitude spikes compared to recording in rodents precluded reliable clustering of putative single neurons, spikes displayed typical waveform patterns (Fig. 4b) and were reliably phase-modulated by cortical slow oscillations (Fig. 4e), confirming the physiologic nature of the activity.

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