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Segregation of cortical head direction cell assemblies on alternating theta cycles

Nature Neuroscience volume 16, pages 739–748 (2013)Cite this article

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Abstract

High-level cortical systems for spatial navigation, including entorhinal grid cells, critically depend on input from the head direction system. We examined spiking rhythms and modes of synchrony between neurons participating in head direction networks for evidence of internal processing, independent of direct sensory drive, which may be important for grid cell function. We found that head direction networks of rats were segregated into at least two populations of neurons firing on alternate theta cycles (theta cycle skipping) with fixed synchronous or anti-synchronous relationships. Pairs of anti-synchronous theta cycle skipping neurons exhibited larger differences in head direction tuning, with a minimum difference of 40 degrees of head direction. Septal inactivation preserved the head direction signal, but eliminated theta cycle skipping of head direction cells and grid cell spatial periodicity. We propose that internal mechanisms underlying cycle skipping in head direction networks may be critical for downstream spatial computation by grid cells.

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Figure 1: Theta cycle skipping covaries positively with head direction tuning.
Figure 2: Characteristics of theta cycle skipping.
Figure 3: Segregation of assemblies on alternating theta cycles.
Figure 4: Characteristics of synchronous and anti-synchronous theta cycle skipping pairs.
Figure 5: Possible downstream functional implications of theta skipping head direction cells.
Figure 6: In vitro theta cycle skipping is reduced with stronger input.
Figure 7: Stronger input can induce theta cycle skipping.

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Acknowledgements

We kindly thank S. Gillet, J. Hinman, E. Newman and L. Ewell for their invaluable consultations and comments on previous versions of this manuscript, as well as M. Connerney, S. Eriksson, C. Libby and T. Ware for technical assistance and behavioral training. This work was supported by grants from the National Institute of Mental Health (R01 MH60013 and MH61492) and the Office of Naval Research Multidisciplinary University Research Initiative (N00014-10-1-0936).

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Author notes

  1. Mark P Brandon & Andrew R Bogaard

    Present address: Present address: Medical Scientist Training Program, University of Washington, Seattle, Washington, USA (A.R.B.), and Center for Neural Circuits and Behavior, Neurobiology Section, Division of Biological Sciences, University of California, San Diego, California, USA (M.P.B.).,

  2. Mark P Brandon and Andrew R Bogaard: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Psychology, Center for Memory and Brain, Graduate Program for Neuroscience, Boston University, Boston, Massachusetts, USA

    Mark P Brandon, Andrew R Bogaard, Nathan W Schultheiss & Michael E Hasselmo

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  1. Mark P Brandon
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Contributions

M.P.B. and M.E.H. designed the in vivo experiments. M.P.B. collected the in vivo data. M.P.B., A.R.B. and N.W.S. designed, and A.R.B. implemented, the in vivo analyses. N.W.S. and M.E.H. designed the in vitro experiments. N.W.S. collected and analyzed the in vitro data. M.E.H. created the network simulations and A.R.B. developed the Poisson model. M.P.B., A.R.B., N.W.S. and M.E.H. wrote the manuscript.

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Correspondence to Mark P Brandon.

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Brandon, M., Bogaard, A., Schultheiss, N. et al. Segregation of cortical head direction cell assemblies on alternating theta cycles. Nat Neurosci 16, 739–748 (2013). https://doi.org/10.1038/nn.3383

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