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Spatial gradients and multidimensional dynamics in a neural integrator circuit

Abstract

In a neural integrator, the variability and topographical organization of neuronal firing-rate persistence can provide information about the circuit's functional architecture. We used optical recording to measure the time constant of decay of persistent firing (persistence time) across a population of neurons comprising the larval zebrafish oculomotor velocity-to-position neural integrator. We found extensive persistence time variation (tenfold; coefficients of variation = 0.58–1.20) across cells in individual larvae. We also found that the similarity in firing between two neurons decreased as the distance between them increased and that a gradient in persistence time was mapped along the rostrocaudal and dorsoventral axes. This topography is consistent with the emergence of persistence time heterogeneity from a circuit architecture in which nearby neurons are more strongly interconnected than distant ones. Integrator circuit models characterized by multiple dimensions of slow firing-rate dynamics can account for our results.

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Figure 1: Potential dynamical and spatial structure among hVPNI neurons.
Figure 2: Saccade-related calcium fluctuations in optically identified hindbrain somata.
Figure 3: NpHR-mediated silencing of the caudal hindbrain reduces eye position stability.
Figure 4: The distribution of persistence time ranges in individual larvae.
Figure 5: Agreement between electrical and optical recording–based parameterizations of saccade-related activity.
Figure 6: Activity correlations between cells depend on their pairwise distance.
Figure 7: Persistence time and response index similarity depend on pairwise distance along spatial dimensions.
Figure 8: Mechanistic implications of heterogeneity in dynamics.

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Acknowledgements

We thank D. Dombeck for technical advice, F. Collman for motion-correction software, and M. Goldman, A. Kinkhabwala and P. Bradley for helpful discussions. This work was supported by a National Science Foundation predoctoral fellowship (A.M.), a US National Institutes of Health Training grant (EY007138-16, K.D.), a Krevans fellowship (A.B.A.), a Burroughs Wellcome Career Award at the Scientific Interface, a Searle Scholar award, the Frueauff Foundation (E.A.), the Human Frontier Science Program (H.B.), and US National Institutes of Health grants (R01 MH060651 to D.W.T. and R01 NS053358 to H.B.).

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Contributions

A.M. collected functional imaging and electrical recording data under the supervision of D.W.T.; A.M., E.A. and D.W.T. developed the preparation, experimental procedures and instrumentation for the imaging and electrophysiological studies; A.M. and K.D. analyzed this data with guidance from E.A. and D.W.T.; A.B.A. and H.B. designed the NpHR study; A.B.A. collected and analyzed the NpHR data; and A.M., K.D., E.A. and D.W.T. wrote the paper.

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Correspondence to Emre Aksay or David W Tank.

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Miri, A., Daie, K., Arrenberg, A. et al. Spatial gradients and multidimensional dynamics in a neural integrator circuit. Nat Neurosci 14, 1150–1159 (2011). https://doi.org/10.1038/nn.2888

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