A ubiquitous spectrolaminar motif of local field potential power across the primate cortex

Diego Mendoza-Halliday; Alex James Major; Noah Lee; Maxwell J Lichtenfeld; Brock Carlson; Blake Mitchell; Patrick D Meng; Yihan Sophy Xiong; Jacob A Westerberg; Xiaoxuan Jia; Kevin D Johnston; Janahan Selvanayagam; Stefan Everling; Alexander Maier; Robert Desimone; Earl K Miller; André M Bastos

doi:10.1038/s41593-023-01554-7

A ubiquitous spectrolaminar motif of local field potential power across the primate cortex

Diego Mendoza-Halliday, Alex James Major, Noah Lee, Maxwell J Lichtenfeld, Brock Carlson, Blake Mitchell, Patrick D Meng, Yihan Sophy Xiong, Jacob A Westerberg, Xiaoxuan Jia, Kevin D Johnston, Janahan Selvanayagam, Stefan Everling, Alexander Maier, Robert Desimone, Earl K Miller, André M Bastos

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Abstract

The mammalian cerebral cortex is anatomically organized into a six-layer motif. It is currently unknown whether a corresponding laminar motif of neuronal activity patterns exists across the cortex. Here we report such a motif in the power of local field potentials (LFPs). Using laminar probes, we recorded LFPs from 14 cortical areas across the cortical hierarchy in five macaque monkeys. The laminar locations of recordings were histologically identified by electrolytic lesions. Across all areas, we found a ubiquitous spectrolaminar pattern characterized by an increasing deep-to-superficial layer gradient of high-frequency power peaking in layers 2/3 and an increasing superficial-to-deep gradient of alpha-beta power peaking in layers 5/6. Laminar recordings from additional species showed that the spectrolaminar pattern is highly preserved among primates-macaque, marmoset and human-but more dissimilar in mouse. Our results suggest the existence of a canonical layer-based and frequency-based mechanism for cortical computation.

Original language	English
Pages (from-to)	547-560
Journal	Nature Neuroscience
Volume	27
DOIs	https://doi.org/10.1038/s41593-023-01554-7
Publication status	Published - 18 Jan 2024

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Mendoza-Halliday, D., Major, A. J., Lee, N., Lichtenfeld, M. J., Carlson, B., Mitchell, B., Meng, P. D., Xiong, Y. S., Westerberg, J. A., Jia, X., Johnston, K. D., Selvanayagam, J., Everling, S., Maier, A., Desimone, R., Miller, E. K., & Bastos, A. M. (2024). A ubiquitous spectrolaminar motif of local field potential power across the primate cortex. Nature Neuroscience, 27, 547-560. https://doi.org/10.1038/s41593-023-01554-7

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title = "A ubiquitous spectrolaminar motif of local field potential power across the primate cortex",

abstract = "The mammalian cerebral cortex is anatomically organized into a six-layer motif. It is currently unknown whether a corresponding laminar motif of neuronal activity patterns exists across the cortex. Here we report such a motif in the power of local field potentials (LFPs). Using laminar probes, we recorded LFPs from 14 cortical areas across the cortical hierarchy in five macaque monkeys. The laminar locations of recordings were histologically identified by electrolytic lesions. Across all areas, we found a ubiquitous spectrolaminar pattern characterized by an increasing deep-to-superficial layer gradient of high-frequency power peaking in layers 2/3 and an increasing superficial-to-deep gradient of alpha-beta power peaking in layers 5/6. Laminar recordings from additional species showed that the spectrolaminar pattern is highly preserved among primates-macaque, marmoset and human-but more dissimilar in mouse. Our results suggest the existence of a canonical layer-based and frequency-based mechanism for cortical computation.",

author = "Diego Mendoza-Halliday and Major, {Alex James} and Noah Lee and Lichtenfeld, {Maxwell J} and Brock Carlson and Blake Mitchell and Meng, {Patrick D} and Xiong, {Yihan Sophy} and Westerberg, {Jacob A} and Xiaoxuan Jia and Johnston, {Kevin D} and Janahan Selvanayagam and Stefan Everling and Alexander Maier and Robert Desimone and Miller, {Earl K} and Bastos, {Andr{\'e} M}",

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doi = "10.1038/s41593-023-01554-7",

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Mendoza-Halliday, D, Major, AJ, Lee, N, Lichtenfeld, MJ, Carlson, B, Mitchell, B, Meng, PD, Xiong, YS, Westerberg, JA, Jia, X, Johnston, KD, Selvanayagam, J, Everling, S, Maier, A, Desimone, R, Miller, EK & Bastos, AM 2024, 'A ubiquitous spectrolaminar motif of local field potential power across the primate cortex', Nature Neuroscience, vol. 27, pp. 547-560. https://doi.org/10.1038/s41593-023-01554-7

TY - JOUR

T1 - A ubiquitous spectrolaminar motif of local field potential power across the primate cortex

AU - Mendoza-Halliday, Diego

AU - Major, Alex James

AU - Lee, Noah

AU - Lichtenfeld, Maxwell J

AU - Carlson, Brock

AU - Mitchell, Blake

AU - Meng, Patrick D

AU - Xiong, Yihan Sophy

AU - Westerberg, Jacob A

AU - Jia, Xiaoxuan

AU - Johnston, Kevin D

AU - Selvanayagam, Janahan

AU - Everling, Stefan

AU - Maier, Alexander

AU - Desimone, Robert

AU - Miller, Earl K

AU - Bastos, André M

PY - 2024/1/18

Y1 - 2024/1/18

N2 - The mammalian cerebral cortex is anatomically organized into a six-layer motif. It is currently unknown whether a corresponding laminar motif of neuronal activity patterns exists across the cortex. Here we report such a motif in the power of local field potentials (LFPs). Using laminar probes, we recorded LFPs from 14 cortical areas across the cortical hierarchy in five macaque monkeys. The laminar locations of recordings were histologically identified by electrolytic lesions. Across all areas, we found a ubiquitous spectrolaminar pattern characterized by an increasing deep-to-superficial layer gradient of high-frequency power peaking in layers 2/3 and an increasing superficial-to-deep gradient of alpha-beta power peaking in layers 5/6. Laminar recordings from additional species showed that the spectrolaminar pattern is highly preserved among primates-macaque, marmoset and human-but more dissimilar in mouse. Our results suggest the existence of a canonical layer-based and frequency-based mechanism for cortical computation.

AB - The mammalian cerebral cortex is anatomically organized into a six-layer motif. It is currently unknown whether a corresponding laminar motif of neuronal activity patterns exists across the cortex. Here we report such a motif in the power of local field potentials (LFPs). Using laminar probes, we recorded LFPs from 14 cortical areas across the cortical hierarchy in five macaque monkeys. The laminar locations of recordings were histologically identified by electrolytic lesions. Across all areas, we found a ubiquitous spectrolaminar pattern characterized by an increasing deep-to-superficial layer gradient of high-frequency power peaking in layers 2/3 and an increasing superficial-to-deep gradient of alpha-beta power peaking in layers 5/6. Laminar recordings from additional species showed that the spectrolaminar pattern is highly preserved among primates-macaque, marmoset and human-but more dissimilar in mouse. Our results suggest the existence of a canonical layer-based and frequency-based mechanism for cortical computation.

U2 - 10.1038/s41593-023-01554-7

DO - 10.1038/s41593-023-01554-7

M3 - Article

C2 - 38238431

SN - 1097-6256

VL - 27

SP - 547

EP - 560

JO - Nature Neuroscience

JF - Nature Neuroscience

ER -

A ubiquitous spectrolaminar motif of local field potential power across the primate cortex

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