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Hippocampal CA1 pyramidal cells form functionally distinct sublayers

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Mizuseki, Kenji, Diba, Kamran, Pastalkova, Eva, Buzsáki, György·2011·Nature Neuroscience
DOI 10.1038/nn.2894
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Abstract

Hippocampal CA1 pyramidal neurons have frequently been regarded as a homogeneous cell population in biophysical, pharmacological and modeling studies. We found robust differences between pyramidal neurons residing in the deep and superficial CA1 sublayers in rats. Compared with their superficial peers, deep pyramidal cells fired at higher rates, burst more frequently, were more likely to have place fields and were more strongly modulated by slow oscillations of sleep. Both deep and superficial pyramidal cells fired preferentially at the trough of theta oscillations during maze exploration, whereas deep pyramidal cells shifted their preferred phase of firing to the peak of theta during rapid eye movement (REM) sleep. Furthermore, although the majority of REM theta phase-shifting cells fired at the ascending phase of gamma oscillations during waking, nonshifting cells preferred the trough. Thus, CA1 pyramidal cells in adjacent sublayers can address their targets jointly or differentially, depending on brain states.

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Research works printed but not linked: 36

  1. Freund, T.F. & Buzsaki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996). · DOI · Paper page
  2. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008). · DOI · Paper page
  3. Connors, B.W., Gutnick, M.J. & Prince, D.A. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48, 1302–1320 (1982). · DOI · Paper page
  4. Chagnac-Amitai, Y., Luhmann, H.J. & Prince, D.A. Burst generating and regular spiking layer 5 pyramidal neurons of rat neocortex have different morphological features. J. Comp. Neurol. 296, 598–613 (1990). · DOI · Paper page
  5. Mason, A. & Larkman, A. Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. J. Neurosci. 10, 1415–1428 (1990). · DOI · Paper page
  6. Yoshimura, Y., Dantzker, J.L. & Callaway, E.M. Excitatory cortical neurons form fine-scale functional networks. Nature 433, 868–873 (2005). · DOI · Paper page
  7. Thomson, A.M., West, D.C., Wang, Y. & Bannister, A.P. Synaptic connections and small circuits involving excitatory and inhibitory neurons in layers 2–5 of adult rat and cat neocortex: triple intracellular recordings and biocytin labeling in vitro. Cereb. Cortex 12, 936–953 (2002). · DOI · Paper page
  8. Deguchi, Y., Donato, F., Galimberti, I., Cabuy, E. & Caroni, P. Temporally matched subpopulations of selectively interconnected principal neurons in the hippocampus. Nat. Neurosci. 14, 495–504 (2011). · DOI · Paper page
  9. Amaral, D. & Lavenex, P. Hippocampal Neuroanatomy. in The Hippocampus Book (Andersen, P., Morris, R., Amaral, D., Bliss, T.V.P. & O'Keefe, J., eds.) 37–114 (Oxford University Press, 2007). · DOI
  10. Tamamaki, N. & Nojyo, Y. Preservation of topography in the connections between the subiculum, field CA1, and the entorhinal cortex in rats. J. Comp. Neurol. 353, 379–390 (1995). · DOI · Paper page
  11. Jarsky, T., Mady, R., Kennedy, B. & Spruston, N. Distribution of bursting neurons in the CA1 region and the subiculum of the rat hippocampus. J. Comp. Neurol. 506, 535–547 (2008). · DOI
  12. Henriksen, E.J. et al. Spatial representation along the proximodistal axis of CA1. Neuron 68, 127–137 (2010). · DOI · Paper page
  13. Golding, N.L., Kath, W.L. & Spruston, N. Dichotomy of action-potential backpropagation in CA1 pyramidal neuron dendrites. J. Neurophysiol. 86, 2998–3010 (2001). · DOI · Paper page
  14. Senior, T.J., Huxter, J.R., Allen, K., O'Neill, J. & Csicsvari, J. Gamma oscillatory firing reveals distinct populations of pyramidal cells in the CA1 region of the hippocampus. J. Neurosci. 28, 2274–2286 (2008). · DOI · Paper page
  15. Bannister, N.J. & Larkman, A.U. Dendritic morphology of CA1 pyramidal neurones from the rat hippocampus. I. Branching patterns. J. Comp. Neurol. 360, 150–160 (1995). · DOI
  16. Baimbridge, K.G., Peet, M.J., McLennan, H. & Church, J. Bursting response to current-evoked depolarization in rat CA1 pyramidal neurons is correlated with lucifer yellow dye coupling but not with the presence of calbindin-D28k. Synapse 7, 269–277 (1991). · DOI
  17. Slomianka, L. Neurons of origin of zinc-containing pathways and the distribution of zinc-containing boutons in the hippocampal region of the rat. Neuroscience 48, 325–352 (1992). · DOI · Paper page
  18. Dong, H.W., Swanson, L.W., Chen, L., Fanselow, M.S. & Toga, A.W. Genomic-anatomic evidence for distinct functional domains in hippocampal field CA1. Proc. Natl. Acad. Sci. USA 106, 11794–11799 (2009). · DOI · Paper page
  19. Csicsvari, J. et al. Massively parallel recording of unit and local field potentials with silicon-based electrodes. J. Neurophysiol. 90, 1314–1323 (2003). · DOI · Paper page
  20. Ylinen, A. et al. Sharp wave–associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J. Neurosci. 15, 30–46 (1995). · DOI · Paper page
  21. Lorente de Nó, R. Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. (Lpz) 46, 113–177 (1934).
  22. Harris, K.D., Hirase, H., Leinekugel, X., Henze, D.A. & Buzsaki, G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141–149 (2001). · DOI · Paper page
  23. Poe, G.R., Nitz, D.A., McNaughton, B.L. & Barnes, C.A. Experience-dependent phase-reversal of hippocampal neuron firing during REM sleep. Brain Res. 855, 176–180 (2000). · DOI · Paper page
  24. Mehta, M.R., Lee, A.K. & Wilson, M.A. Role of experience and oscillations in transforming a rate code into a temporal code. Nature 417, 741–746 (2002). · DOI · Paper page
  25. O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971). · DOI · Paper page
  26. Muller, R.U. & Kubie, J.L. The firing of hippocampal place cells predicts the future position of freely moving rats. J. Neurosci. 9, 4101–4110 (1989). · DOI · Paper page
  27. Hafting, T., Fyhn, M., Bonnevie, T., Moser, M.B. & Moser, E.I. Hippocampus-independent phase precession in entorhinal grid cells. Nature 453, 1248–1252 (2008). · DOI · Paper page
  28. Skaggs, W.E., McNaughton, B.L., Gothard, K.M. & Markus, E.J. An information-theoretic approach to deciphering the hippocampal code. in Advances in Neural Information Processing Systems, vol. 5 (Hanson, S.J., Cowan, J.D. & Giles C.L., eds.) 1030–1037 (Morgan Kaufmann, 1993).
  29. Skaggs, W.E., McNaughton, B.L., Wilson, M.A. & Barnes, C.A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6, 149–172 (1996). · doi:10.1002/(sici)1098-1063(1996)6:2<149::aid-hipo6>3.0.co;2-k
  30. Markus, E.J., Barnes, C.A., McNaughton, B.L., Gladden, V.L. & Skaggs, W.E. Spatial information content and reliability of hippocampal CA1 neurons: effects of visual input. Hippocampus 4, 410–421 (1994). · DOI · Paper page
  31. O'Keefe, J. & Recce, M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993). · DOI · Paper page
  32. Csicsvari, J., Jamieson, B., Wise, K.D. & Buzsaki, G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311–322 (2003). · DOI · Paper page
  33. Peters, S., Koh, J. & Choi, D.W. Zinc selectively blocks the action of N-methyl-D-aspartate on cortical neurons. Science 236, 589–593 (1987). · DOI · Paper page
  34. Molinari, S. et al. Deficits in memory and hippocampal long-term potentiation in mice with reduced calbindin D28K expression. Proc. Natl. Acad. Sci. USA 93, 8028–8033 (1996). · DOI · Paper page
  35. Sørensen, J.C., Tonder, N. & Slomianka, L. Zinc-positive afferents to the rat septum originate from distinct subpopulations of zinc-containing neurons in the hippocampal areas and layers. A combined fluoro-gold tracing and histochemical study. Anat. Embryol. (Berl.) 188, 107–115 (1993). · DOI
  36. Bilkey, D.K. & Schwartzkroin, P.A. Variation in electrophysiology and morphology of hippocampal CA3 pyramidal cells. Brain Res. 514, 77–83 (1990). · DOI

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Metadata

Authors
Mizuseki, K., Diba, K., Pastalkova, E., & Buzsáki, G.
Venue
Nature Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2011-08-07
Volume
14
Issue
9
Pages
1174-1181
ISSN
  • 1097-6256 (ISSN-L)
  • 1546-1726
DOI
10.1038/nn.2894
OpenAlex
W2070368256
Cited by
461
References
14
FWCI
8.89
Type
journal article
Language
en
Open access
green
Licence
www.springer.com/tdm (tdm)

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Mizuseki, K., Diba, K., Pastalkova, E., & Buzsáki, G. (2011). Hippocampal CA1 pyramidal cells form functionally distinct sublayers. Nature Neuroscience. https://doi.org/10.1038/nn.2894

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