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A morphological basis for orientation tuning in primary visual cortex

Abstract

Feedforward connections are thought to be important in the generation of orientation-selective responses in visual cortex by establishing a bias in the sampling of information from regions of visual space that lie along a neuron's axis of preferred orientation. It remains unclear, however, which structural elements—dendrites or axons—are ultimately responsible for conveying this sampling bias. To explore this question, we have examined the spatial arrangement of feedforward axonal connections that link non-oriented neurons in layer 4 and orientation-selective neurons in layer 2/3 of visual cortex in the tree shrew. Target sites of labeled boutons in layer 2/3 resulting from focal injections of biocytin in layer 4 show an orientation-specific axial bias that is sufficient to confer orientation tuning to layer 2/3 neurons. We conclude that the anisotropic arrangement of axon terminals is the principal source of the orientation bias contributed by feedforward connections.

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Figure 1: Patterns of connections between layer 4 and layer 2/3 neurons predicted by the feedforward model of orientation selectivity.
Figure 2: Focal injections of biocytin into cortical layer 4 label small clusters of layer 4 neurons and their divergent projections to layer 2/3.
Figure 3: Layer 4 projections preferentially target sites in layer 2/3 that show matching orientation preference and axis of displacement.
Figure 4: Correspondence between orientation preference and axis of displacement: dependence on the specificity of axonal connections.
Figure 5: Organization of layer 4 input to layer 2/3 receptive fields.

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Acknowledgements

We thank M. Pucak, A. Basole, H. Chisum, E. Johnson, V. Kreft-Kerekes, T. Tucker and L. White for discussions. This work was supported by grants from the NIH (EY06821) and the Swiss National Science Foundation (81FR-54690).

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Correspondence to David Fitzpatrick.

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Mooser, F., Bosking, W. & Fitzpatrick, D. A morphological basis for orientation tuning in primary visual cortex. Nat Neurosci 7, 872–879 (2004). https://doi.org/10.1038/nn1287

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