Development of neuronal timescales in human cortical organoids and rat hippocampus dissociated cultures

被引:0
作者
Martin-Burgos, Blanca [3 ]
McPherson, Trevor Supan [3 ]
Hammonds, Ryan [1 ,2 ]
Gao, Richard [1 ]
Muotri, Alysson R. [5 ,6 ]
Voytek, Bradley [1 ,2 ,3 ,4 ]
机构
[1] Univ Calif San Diego, Dept Cognit Sci, La Jolla, CA 92093 USA
[2] Univ Calif San Diego, Halicioglu Data Sci Inst, La Jolla, CA 92093 USA
[3] Univ Calif San Diego, Neurosci Grad Program, La Jolla, CA 92093 USA
[4] Univ Calif San Diego, Kavli Inst Brain & Mind, La Jolla, CA 92093 USA
[5] Univ Calif San Diego, Rady Childrens Hosp San Diego, Sch Med, Dept Pediat, La Jolla, CA 92093 USA
[6] Univ Calif San Diego, Sch Med, Dept Cellular & Mol Med, La Jolla, CA 92093 USA
关键词
cortical organoids; development; local field potentials; rodent hippocampal dissociated cultures; neuronal timescales; MATURATION; DYNAMICS;
D O I
10.1152/jn.00135.2024
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
To support complex cognition, neuronal circuits must integrate information across multiple temporal scales, ranging from milliseconds to decades. Neuronal timescales describe the duration over which activity within a network persists, posing a putative explanatory mechanism for how information might be integrated over multiple temporal scales. Little is known about how timescales develop in human neural circuits or other model systems, limiting insight into how the functional dynamics necessary for cognition emerge. In our work, we show that neuronal timescales develop in a nonlinear fashion in human cortical organoids, which is partially replicated in dissociated rat hippocampus cultures. We use spectral parameterization of spiking activity to extract an estimate of neuronal timescale that is unbiased by coevolving oscillations. Cortical organoid timescales begin to increase around month 6 postdifferentiation. In rodent hippocampal dissociated cultures, we see that timescales decrease from in vitro days 13-23 before stabilizing. We speculate that cortical organoid development over the duration studied here reflects an earlier stage of a generalized developmental timeline in contrast to the rodent hippocampal cultures, potentially accounting for differences in timescale developmental trajectories. The fluctuation of timescales might be an important developmental feature that reflects the changing complexity and information capacity in developing neuronal circuits. NEW & NOTEWORTHY Neuronal timescales describe the persistence of activity within a network of neurons. Timescales were found to fluctuate with development in two model systems. In cortical organoids timescales increased, peaked, and then decreased throughout development; in rat hippocampal dissociated cultures timescales decreased over development. These distinct developmental models overlap to highlight a critical window in which timescales lengthen and contract, potentially indexing changes in the information capacity of neuronal systems.
引用
收藏
页码:757 / 764
页数:8
相关论文
共 36 条
[1]   Brain Organoids as Tools for Modeling Human Neurodevelopmental Disorders [J].
Adams, Jason W. ;
Cugola, Fernanda R. ;
Muotri, Alysson R. .
PHYSIOLOGY, 2019, 34 (05) :365-375
[2]   A functional hiPSC-cortical neuron differentiation and maturation model and its application to neurological disorders [J].
Autar, Kaveena ;
Guo, Xiufang ;
Rumsey, John W. ;
Long, Christopher J. ;
Akanda, Nesar ;
Jackson, Max ;
Narasimhan, Narasimhan S. ;
Caneus, Julbert ;
Morgan, Dave ;
Hickman, James J. .
STEM CELL REPORTS, 2022, 17 (01) :96-109
[3]   A Diversity of Intrinsic Timescales Underlie Neural Computations [J].
Cavanagh, Sean E. ;
Hunt, Laurence T. ;
Kennerley, Steven W. .
FRONTIERS IN NEURAL CIRCUITS, 2020, 14
[4]   Neural Intrinsic Timescales in the Macaque Dorsal Premotor Cortex Predict the Strength of Spatial Response Coding [J].
Cirillo, Rossella ;
Fascianelli, Valeria ;
Ferrucci, Lorenzo ;
Genovesio, Aldo .
ISCIENCE, 2018, 10 :203-+
[5]  
Cole S., 2019, J Open Source Softw, V4, P1272, DOI [10.21105/joss.01272, DOI 10.21105/JOSS.01272]
[6]   Parameterizing neural power spectra into periodic and aperiodic components [J].
Donoghue, Thomas ;
Haller, Matar ;
Peterson, Erik J. ;
Varma, Paroma ;
Sebastian, Priyadarshini ;
Gao, Richard ;
Noto, Torben ;
Lara, Antonio H. ;
Wallis, Joni D. ;
Knight, Robert T. ;
Shestyuk, Avgusta ;
Voytek, Bradley .
NATURE NEUROSCIENCE, 2020, 23 (12) :1655-U288
[7]   Synaptic patterning and the timescales of cortical dynamics [J].
Duarte, Renato ;
Seeholzer, Alexander ;
Zilles, Karl ;
Morrison, Abigail .
CURRENT OPINION IN NEUROBIOLOGY, 2017, 43 :156-165
[8]   Neuronal timescales are functionally dynamic and shaped by cortical microarchitecture [J].
Gao, Richard ;
van den Brink, Ruud L. ;
Pfeffer, Thomas ;
Voytek, Bradley .
ELIFE, 2020, 9 :1-44
[9]   The brain and its time: intrinsic neural timescales are key for input processing [J].
Golesorkhi, Mehrshad ;
Gomez-Pilar, Javier ;
Zilio, Federico ;
Berberian, Nareg ;
Wolff, Annemarie ;
Yagoub, Mustapha C. E. ;
Northoff, Georg .
COMMUNICATIONS BIOLOGY, 2021, 4 (01)
[10]   Long-term maturation of human cortical organoids matches key early postnatal transitions [J].
Gordon, Aaron ;
Yoon, Se-Jin ;
Tran, Stephen S. ;
Makinson, Christopher D. ;
Park, Jin Young ;
Andersen, Jimena ;
Valencia, Alfredo M. ;
Horvath, Steve ;
Xiao, Xinshu ;
Huguenard, John R. ;
Pasca, Sergiu P. ;
Geschwind, Daniel H. .
NATURE NEUROSCIENCE, 2021, 24 (03) :331-342