What we can learn from the complex architecture of single axons

Abstract

Anterogradely labeled connections at the single-axon level provide unparalleled spatial and quantitative data as well as a novel perspective on laminar, columnar, hierarchical and other aspects of cortical organization. Here, I briefly summarize single-axon results from representative examples of thalamocortical, corticocortical, callosal, and lateral intrinsic connections, with attention to implications for cortical organization. Particularly worth emphasizing is the intricate spatial configuration and striking morphometric heterogeneity of individual axons even within the same system of connections. A short section touches on patterns of axonal trajectories in the distal, preterminal few millimeters. Emphasis is on studies in nonhuman primates from about 1983 to present, with non-viral tracers and 2-D reconstruction (i.e., compressed z-axis) in the early visual cortical pathway. The last section recapitulates what this approach can tell us about inter-areal communication and cortical organization, and possible implications for dynamics and effective connectivity, and concludes with comments on open questions and future directions.

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Fig. 1
Fig. 2

Adapted with permission from Rockland et al. (1999)

Fig. 3

Adapted with permission from Rockland et al. (1999)

Fig. 4
Fig. 5

Adapted with permission from Rockland (1992)

Fig. 6

Adapted with permission from Rockland (1995)

Fig. 7

Adapted with permission from Rockland (2002a)

Fig. 8

Adapted with permission from Rockland and Knutson (2000)

Fig. 9

Adapted with permission from Rockland (2002a)

Fig. 10

Adapted with permission from Martin et al. (2014)

Fig. 11

Adapted with permission from Rockland (1994) and Freund et al. (1989)

Fig. 12

Adapted with permission from Rockland et al. (1994)

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Acknowledgements

I thank Drs. Jennifer Luebke, Farzad Mortazavi, Mihovil Pletikos, and R. Jarrett Rushmore for reading the manuscript and for helpful discussion.

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No funding has been received for the present work by the author(ksr). As this is a review paper, issues of informed consent and of treatment of human (not applicable) or animal subjects do not apply. Animal work had been approved at several relevant institutions (Boston University, U. of Iowa, or RIKEN Brain Science Institute) as stated in the original research papers. Credit has been explicitly given to any original research mentioned in the paper.

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Correspondence to Kathleen S. Rockland.

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Rockland, K.S. What we can learn from the complex architecture of single axons. Brain Struct Funct 225, 1327–1347 (2020). https://doi.org/10.1007/s00429-019-02023-3

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Keywords

  • Cortical columns
  • Distributed
  • Feedback
  • Divergence
  • Feedforward
  • Cortical layers
  • Multi-scale
  • Trajectory