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Chronic recordings from the marmoset motor cortex reveals modulation of neural firing and local field potentials overlap with macaques.

ABSTRACT: Objective.The common marmoset has been increasingly used in neural interfacing studies due to its smaller size, easier handling, and faster breeding compared to Old World non-human primate (NHP) species. While assessment of cortical anatomy in marmosets has shown strikingly similar layout to macaques, comprehensive assessment of electrophysiological properties underlying forelimb reaching movements in this bridge species does not exist. The objective of this study is to characterize electrophysiological properties of signals recorded from the marmoset primary motor cortex (M1) during a reach task and compare with larger NHP models such that this smaller NHP model can be used in behavioral neural interfacing studies.Approach and main results.Neuronal firing rates and local field potentials (LFPs) were chronically recorded from M1 in three adult, male marmosets. Firing rates, mu + beta and high gamma frequency bands of LFPs were evaluated for modulation with respect to movement. Firing rate and regularity of neurons of the marmoset M1 were similar to that reported in macaques with a subset of neurons showing selectivity to movement direction. Movement phases (rest vs move) was classified from both neural spiking and LFPs. Microelectrode arrays provide the ability to sample small regions of the motor cortex to drive brain-machine interfaces (BMIs). The results demonstrate that marmosets are a robust bridge species for behavioral neuroscience studies with motor cortical electrophysiological signals recorded from microelectrode arrays that are similar to Old World NHPs.Significance. As marmosets represent an interesting step between rodent and macaque models, successful demonstration that neuron modulation in marmoset motor cortex is analogous to reports in macaques illustrates the utility of marmosets as a viable species for BMI studies.

SUBMITTER: Mylavarapu R

PROVIDER: S-EPMC8612807 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Objective. Electrical recordings of neural activity from brain surface have been widely employed in basic neuroscience research and clinical practice for investigations of neural circuit functions, brain-computer interfaces, and treatments for neurological disorders. Traditionally, these surface potentials have been believed to mainly reflect local neural activity. It is not known how informative the locally recorded surface potentials are for the neural activities across multiple cortical regions.Approach. To investigate that, we perform simultaneous local electrical recording and wide-field calcium imaging in awake head-fixed mice. Using a recurrent neural network model, we try to decode the calcium fluorescence activity of multiple cortical regions from local electrical recordings.Main results. The mean activity of different cortical regions could be decoded from locally recorded surface potentials. Also, each frequency band of surface potentials differentially encodes activities from multiple cortical regions so that including all the frequency bands in the decoding model gives the highest decoding performance. Despite the close spacing between recording channels, surface potentials from different channels provide complementary information about the large-scale cortical activity and the decoding performance continues to improve as more channels are included. Finally, we demonstrate the successful decoding of whole dorsal cortex activity at pixel-level using locally recorded surface potentials.Significance. These results show that the locally recorded surface potentials indeed contain rich information of the large-scale neural activities, which could be further demixed to recover the neural activity across individual cortical regions. In the future, our cross-modality inference approach could be adapted to virtually reconstruct cortex-wide brain activity, greatly expanding the spatial reach of surface electrical recordings without increasing invasiveness. Furthermore, it could be used to facilitate imaging neural activity across the whole cortex in freely moving animals, without requirement of head-fixed microscopy configurations.

Project description:OBJECTIVE:Action potentials and local field potentials (LFPs) recorded in primary motor cortex contain information about the direction of movement. LFPs are assumed to be more robust to signal instabilities than action potentials, which makes LFPs, along with action potentials, a promising signal source for brain-computer interface applications. Still, relatively little research has directly compared the utility of LFPs to action potentials in decoding movement direction in human motor cortex. APPROACH:We conducted intracortical multi-electrode recordings in motor cortex of two persons (T2 and [S3]) as they performed a motor imagery task. We then compared the offline decoding performance of LFPs and spiking extracted from the same data recorded across a one-year period in each participant. MAIN RESULTS:We obtained offline prediction accuracy of movement direction and endpoint velocity in multiple LFP bands, with the best performance in the highest (200-400 Hz) LFP frequency band, presumably also containing low-pass filtered action potentials. Cross-frequency correlations of preferred directions and directional modulation index showed high similarity of directional information between action potential firing rates (spiking) and high frequency LFPs (70-400 Hz), and increasing disparity with lower frequency bands (0-7, 10-40 and 50-65 Hz). Spikes predicted the direction of intended movement more accurately than any individual LFP band, however combined decoding of all LFPs was statistically indistinguishable from spike-based performance. As the quality of spiking signals (i.e. signal amplitude) and the number of significantly modulated spiking units decreased, the offline decoding performance decreased 3.6[5.65]%/month (for T2 and [S3] respectively). The decrease in the number of significantly modulated LFP signals and their decoding accuracy followed a similar trend (2.4[2.85]%/month, ANCOVA, p = 0.27[0.03]). SIGNIFICANCE:Field potentials provided comparable offline decoding performance to unsorted spikes. Thus, LFPs may provide useful external device control using current human intracortical recording technology. ( CLINICAL TRIAL REGISTRATION NUMBER:NCT00912041.).

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Chronic recordings from the marmoset motor cortex reveals modulation of neural firing and local field potentials overlap with macaques.

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