TY - JOUR
T1 - Simultaneously determining regional heterogeneity and connection directionality from neural activity and symmetric connection
AU - Chang, Jiawen
AU - Yang, Zhuda
AU - Zhou, Changsong
N1 - This work was partially supported by Science and Technology Innovation 2030-Major Projects (No. 2022ZD0208500 to C.Z.), the Hong Kong Research Grant Council (RGC) Senior Research Fellow Scheme (SRFS2324-2S05 to C.Z.), General Competitive Fund (GRF12202124 to C.Z.), and Hong Kong Baptist University (HKBU) Seed Funding for Collaborative Research Grants (RC-SFCRG/23-24/SCI/06 to Changsong Zhou). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Publisher Copyright:
© 2025 Chang et al.
PY - 2025/10/23
Y1 - 2025/10/23
N2 - The spatiotemporal patterns of neural dynamics are jointly shaped by directed structural interactions and heterogeneous intrinsic features of the neural components. Despite well-developed methods for estimating directionality in network connections from network of homogeneous nodes, how local heterogeneity impacts on directionality estimation remains poorly understood. In particular, the role of excitatory-inhibitory interactions in shaping network directionality and how these interactions should be incorporated into reconstruction frameworks remain largely unexplored. Here, we present a novel reconstruction framework that simultaneously estimates effective heterogeneity across network nodes and asymmetric network connections from neural activity and symmetric connection, both are assessible in experimental data, validated using macaque cortical connectivity data and several circuit models. We found that the estimated local heterogeneity remains consistent across various forms of parameterized local circuit heterogeneity. Furthermore, we demonstrated and quantified how hidden local inhibitory populations only modify within-region connection strengths, elucidating the functional equivalence between dynamics of excitatory-inhibitory networks and purely observing excitatory networks when estimating effective heterogeneity and asymmetry. Finally, we demonstrated the sampling interval effect in estimating network interactions with respect to the sampling resolution. Together, our results not only provide a unified framework for evaluating relative functional contributions of local heterogeneity and asymmetry to overall system dynamics but also reveal the fundamental limitations and scaling principles in reconstructing neural circuit connectivity from experimental observations.
AB - The spatiotemporal patterns of neural dynamics are jointly shaped by directed structural interactions and heterogeneous intrinsic features of the neural components. Despite well-developed methods for estimating directionality in network connections from network of homogeneous nodes, how local heterogeneity impacts on directionality estimation remains poorly understood. In particular, the role of excitatory-inhibitory interactions in shaping network directionality and how these interactions should be incorporated into reconstruction frameworks remain largely unexplored. Here, we present a novel reconstruction framework that simultaneously estimates effective heterogeneity across network nodes and asymmetric network connections from neural activity and symmetric connection, both are assessible in experimental data, validated using macaque cortical connectivity data and several circuit models. We found that the estimated local heterogeneity remains consistent across various forms of parameterized local circuit heterogeneity. Furthermore, we demonstrated and quantified how hidden local inhibitory populations only modify within-region connection strengths, elucidating the functional equivalence between dynamics of excitatory-inhibitory networks and purely observing excitatory networks when estimating effective heterogeneity and asymmetry. Finally, we demonstrated the sampling interval effect in estimating network interactions with respect to the sampling resolution. Together, our results not only provide a unified framework for evaluating relative functional contributions of local heterogeneity and asymmetry to overall system dynamics but also reveal the fundamental limitations and scaling principles in reconstructing neural circuit connectivity from experimental observations.
UR - https://www.scopus.com/pages/publications/105020625438
U2 - 10.1371/journal.pcbi.1013612
DO - 10.1371/journal.pcbi.1013612
M3 - Journal article
C2 - 41129567
AN - SCOPUS:105020625438
SN - 1553-734X
VL - 21
JO - PLoS Computational Biology
JF - PLoS Computational Biology
IS - 10
M1 - e1013612
ER -