Hierarchical gradients of multiple timescales in the mammalian forebrain

Many anatomical and physiological features of cortical circuits, ranging from the biophysical properties of synapses to the connectivity patterns among different neuron types, exhibit consistent variation along the hierarchical axis from sensory to association areas. Notably, the temporal correlation of neural activity at rest, known as the intrinsic timescale, increases systematically along this hierarchy in both primates and rodents, analogous to the increasing scale and complexity of spatial receptive fields. However, how the timescales for task-related activity vary across brain regions and whether their hierarchical organization appears consistently across different mammalian species remain unexplored. Here, we show that both the intrinsic timescale and those of task-related activity follow a similar hierarchical gradient in the cortices of monkeys, rats, and mice. We also found that these timescales covary similarly in both the cortex and basal ganglia, whereas the timescales of thalamic activity are shorter than cortical timescales and do not conform to the hierarchical order predicted by their cortical projections. These results suggest that the hierarchical gradient of cortical timescales might represent a universal feature of intracortical circuits in the mammalian brain.

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Publication Details

Journal
Proceedings of the National Academy of Sciences
Published
2024-12-13
DOI
https://doi.org/10.1073/pnas.2415695121
Citations
22
Primary Topic
Neural dynamics and brain function
Type
article
Field-Weighted Citation Impact
7.54

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article

Hierarchical gradients of multiple timescales in the mammalian forebrain

Nicholas A. Steinmetz, Hyojung Seo, Se‐Bum Paik, Daeyeol Lee et al.
22 citations
Proceedings of the National Academy of Sciences
Neural dynamics and brain function
7.54
article

Hierarchical gradients of multiple timescales in the mammalian forebrain

Nicholas A. Steinmetz, Hyojung Seo, Se‐Bum Paik, Daeyeol Lee, Alireza Soltani, Min Song, Min Whan Jung, Eun Ju Shin
article en
22 citations

Abstract

Many anatomical and physiological features of cortical circuits, ranging from the biophysical properties of synapses to the connectivity patterns among different neuron types, exhibit consistent variation along the hierarchical axis from sensory to association areas. Notably, the temporal correlation of neural activity at rest, known as the intrinsic timescale, increases systematically along this hierarchy in both primates and rodents, analogous to the increasing scale and complexity of spatial receptive fields. However, how the timescales for task-related activity vary across brain regions and whether their hierarchical organization appears consistently across different mammalian species remain unexplored. Here, we show that both the intrinsic timescale and those of task-related activity follow a similar hierarchical gradient in the cortices of monkeys, rats, and mice. We also found that these timescales covary similarly in both the cortex and basal ganglia, whereas the timescales of thalamic activity are shorter than cortical timescales and do not conform to the hierarchical order predicted by their cortical projections. These results suggest that the hierarchical gradient of cortical timescales might represent a universal feature of intracortical circuits in the mammalian brain.

Proceedings of the National Academy of SciencesVol. 121(51)
Dartmouth College (US), Allen Institute for Brain Science (US), Johns Hopkins University (US), Korea Advanced Institute of Science and Technology (KR), University of Washington (US), Yale University (US), Korea Institute of Brain Science (KR), Institute for Basic Science (KR), Neuroscience Institute (IT), Brain (Germany) (DE)
Yale University, University of Washington, Johns Hopkins University, Dartmouth College, National Research Foundation, National Research Foundation of Korea, Korea Advanced Institute of Science and Technology, Institute for Basic Science, Directorate for Biological Sciences, Department of Psychological and Brain Sciences, Dartmouth College, National Institute of Mental Health, National Institute on Drug Abuse
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Neural dynamics and brain function
7.54
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