TY - JOUR
T1 - Modular strategy for development of the hierarchical visual network in mice
AU - Murakami, Tomonari
AU - Matsui, Teppei
AU - Uemura, Masato
AU - Ohki, Kenichi
N1 - Funding Information:
We thank members of the Ohki laboratory for discussions; A. Honda, Y. Sono, A. Hayashi, T. Inoue, A. Ohmori, M. Saito, Y. Kato, M. Taki, S. Uto and N. Yamamoto for animal care and genotyping; T. Ohmine and N. Yamamoto for lab management; and H. Takeuchi and K.M. Hagihara for comments on the manuscript. We acknowledge support from The Research Support Center, Kyushu University Graduate School of Medical Sciences, and Imaging Core of International Research Center for Neurointelligence (IRCN), The University of Tokyo, Virus Vector Core of the Brain/MINDS-AMED (JP21dm0207111), and GENIE project, the Janelia Farm Research Campus. This work was supported by Brain/MINDS-AMED (14533320, 15653077, JP16dm0207034 and JP20dm0207048 to K.O.); the Institute for AI and Beyond (to K.O.); JSPS KAKENHI (25221001, 19H05642 and 20H05917 to K.O., 17K14931, 18H05116 and 21H0516513 to T. Matsui, and 19K21207 and 21K15181 to T. Murakami); Brain/MINDS-beyond-AMED (JP20dm0307031 to T. Matsui); and JST PRESTO (JPMJPR19M9 to T. Matsui).
Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2022/8/18
Y1 - 2022/8/18
N2 - Hierarchical and parallel networks are fundamental structures of the mammalian brain1–8. During development, lower- and higher-order thalamic nuclei and many cortical areas in the visual system form interareal connections and build hierarchical dorsal and ventral streams9–13. One hypothesis for the development of visual network wiring involves a sequential strategy wherein neural connections are sequentially formed alongside hierarchical structures from lower to higher areas14–17. However, this sequential strategy would be inefficient for building the entire visual network comprising numerous interareal connections. We show that neural pathways from the mouse retina to primary visual cortex (V1) or dorsal/ventral higher visual areas (HVAs) through lower- or higher-order thalamic nuclei form as parallel modules before corticocortical connections. Subsequently, corticocortical connections among V1 and HVAs emerge to combine these modules. Retina-derived activity propagating the initial parallel modules is necessary to establish retinotopic inter-module connections. Thus, the visual network develops in a modular manner involving initial establishment of parallel modules and their subsequent concatenation. Findings in this study raise the possibility that parallel modules from higher-order thalamic nuclei to HVAs act as templates for cortical ventral and dorsal streams and suggest that the brain has an efficient strategy for the development of a hierarchical network comprising numerous areas.
AB - Hierarchical and parallel networks are fundamental structures of the mammalian brain1–8. During development, lower- and higher-order thalamic nuclei and many cortical areas in the visual system form interareal connections and build hierarchical dorsal and ventral streams9–13. One hypothesis for the development of visual network wiring involves a sequential strategy wherein neural connections are sequentially formed alongside hierarchical structures from lower to higher areas14–17. However, this sequential strategy would be inefficient for building the entire visual network comprising numerous interareal connections. We show that neural pathways from the mouse retina to primary visual cortex (V1) or dorsal/ventral higher visual areas (HVAs) through lower- or higher-order thalamic nuclei form as parallel modules before corticocortical connections. Subsequently, corticocortical connections among V1 and HVAs emerge to combine these modules. Retina-derived activity propagating the initial parallel modules is necessary to establish retinotopic inter-module connections. Thus, the visual network develops in a modular manner involving initial establishment of parallel modules and their subsequent concatenation. Findings in this study raise the possibility that parallel modules from higher-order thalamic nuclei to HVAs act as templates for cortical ventral and dorsal streams and suggest that the brain has an efficient strategy for the development of a hierarchical network comprising numerous areas.
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U2 - 10.1038/s41586-022-05045-w
DO - 10.1038/s41586-022-05045-w
M3 - Article
C2 - 35922512
AN - SCOPUS:85135239932
SN - 0028-0836
VL - 608
SP - 578
EP - 585
JO - Nature
JF - Nature
IS - 7923
ER -