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Disentangling the functional consequences of the connectivity between optic-flow processing neurons

Nature Neuroscience volume 15, pages 441–448 (2012)Cite this article

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Abstract

Typically, neurons in sensory areas are highly interconnected. Coupling two neurons can synchronize their activity and affect a variety of single-cell properties, such as their stimulus tuning, firing rate or gain. All of these factors must be considered to understand how two neurons should be coupled to optimally process stimuli. We quantified the functional effect of an interaction between two optic-flow processing neurons (Vi and H1) in the fly (Lucilia sericata). Using a generative model, we estimated a uni-directional coupling from H1 to Vi. Especially at a low signal-to-noise ratio (SNR), the coupling strongly improved the information about optic-flow in Vi. We identified two constraints confining the strength of the interaction. First, for weak couplings, Vi benefited from inputs by H1 without a concomitant shift of its stimulus tuning. Second, at both low and high SNR, the coupling strength lay in a range in which the information carried by single spikes is optimal.

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Figure 1: The responses of the left Vi and right H1 cells are correlated.
Figure 2: Random rotation stimulus.
Figure 3: Generative model for Vi and H1.
Figure 4: GLM components.
Figure 5: H1 enhances the amplitude of Vi's rotation tuning without affecting the tuning shape.
Figure 6: The coupling improves Vi's stimulus representation.
Figure 7: Effect of a fictive coupling from Vi to H1.

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Acknowledgements

We thank E. Schneidman and G. Tkacik for important discussions during the Methods in Computational Neuroscience course in Woods Hole, Massachusetts. We thank M. Walter for improving the functionality of the LED arena, F. Schwarz for help with the experiments and H. Eichner for critically reading the manuscript. F.W. is supported by a grant from the Deutsche Forschungsgemeinschaft (DFG, Research Training Group 1091) and the Max Planck Society. C.K.M. is funded through the Emmy-Noether program of the DFG and a “Chaire d'excellence” of the Agence National de la Recherche.

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Author notes

  1. Christian K. Machens

    Present address: Present address: Champalimaud Neuroscience Program, Champalimaud Foundation, Lisbon, Portugal.,

Authors and Affiliations

  1. Department of Systems and Computational Neurobiology, Max Planck Institute of Neurobiology, Martinsried, Germany

    Franz Weber & Alexander Borst

  2. Graduate School of Systemic Neurosciences, Ludwig Maximilians University, Munich, Germany

    Franz Weber

  3. Département d'Études Cognitives, Group for Neural Theory, INSERM Unité 960, École Normal Supérieure, Paris, France

    Christian K. Machens

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Contributions

F.W., C.K.M. and A.B. designed the study. F.W. performed all of the experiments and analyzed the data. F.W., C.K.M. and A.B. wrote the manuscript.

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Correspondence to Franz Weber.

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Weber, F., Machens, C. & Borst, A. Disentangling the functional consequences of the connectivity between optic-flow processing neurons. Nat Neurosci 15, 441–448 (2012). https://doi.org/10.1038/nn.3044

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