Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition (original) (raw)

References

  1. Freund, T.F. & Buzsáki, G. Interneurons of the hippocampus. Hippocampus 6, 347–470 (1996).
    Article CAS Google Scholar
  2. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).
    Article CAS Google Scholar
  3. Markram, H. et al. Interneurons of the neocortical inhibitory system. Nat. Rev. Neurosci. 5, 793–807 (2004).
    Article CAS Google Scholar
  4. Isaacson, J.S. & Scanziani, M. How inhibition shapes cortical activity. Neuron 72, 231–243 (2011).
    Article CAS Google Scholar
  5. Klausberger, T. et al. Brain state– and cell type–specific firing of hippocampal interneurons in vivo. Nature 421, 844–848 (2003).
    Article CAS Google Scholar
  6. Cardin, J.A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663–667 (2009).
    Article CAS Google Scholar
  7. Csicsvari, J., Hirase, H., Czurkó, A., Mamiya, A. & Buzsáki, G. Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J. Neurosci. 19, 274–287 (1999).
    Article CAS Google Scholar
  8. Runyan, C.A. et al. Response features of parvalbumin-expressing interneurons suggest precise roles for subtypes of inhibition in visual cortex. Neuron 67, 847–857 (2010).
    Article CAS Google Scholar
  9. Sillito, A.M. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Physiol. (Lond.) 250, 305–329 (1975).
    Article CAS Google Scholar
  10. Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).
    Article CAS Google Scholar
  11. O'Keefe, J. Hippocampal neurophysiology in the behaving animal. in The Hippocampus Book (eds. Andersen, P., Morris, R.G.M., Amaral, D.G., Bliss, T.V.P. & O'Keefe, J.) 475–548 (Oxford, Oxford Neuroscience, 2006).
  12. McNaughton, B.L., Battaglia, F.P., Jensen, O., Moser, E.I. & Moser, M.B. Path integration and the neural basis of the 'cognitive map'. Nat. Rev. Neurosci. 7, 663–678 (2006).
    Article CAS Google Scholar
  13. Ranck, J.B. Jr. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp. Neurol. 41, 461–531 (1973).
    Article Google Scholar
  14. O'Keefe, J. & Recce, M.L. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3, 317–330 (1993).
    Article CAS Google Scholar
  15. Jensen, O. & Lisman, J.E. Hippocampal CA3 region predicts memory sequences: accounting for the phase precession of place cells. Learn. Mem. 3, 279–287 (1996).
    Article CAS Google Scholar
  16. 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).
    Article CAS Google Scholar
  17. Dragoi, G. & Buzsáki, G. Temporal encoding of place sequences by hippocampal cell assemblies. Neuron 50, 145–157 (2006).
    Article CAS Google Scholar
  18. Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003).
    Article CAS Google Scholar
  19. Huxter, J.R., Senior, T.J., Allen, K. & Csicsvari, J. Theta phase–specific codes for two-dimensional position, trajectory and heading in the hippocampus. Nat. Neurosci. 11, 587–594 (2008).
    Article CAS Google Scholar
  20. Geisler, C. et al. Temporal delays among place cells determine the frequency of population theta oscillations in the hippocampus. Proc. Natl. Acad. Sci. USA 107, 7957–7962 (2010).
    Article CAS Google Scholar
  21. Kamondi, A., Acsády, L., Wang, X.J. & Buzsáki, G. Theta oscillations in somata and dendrites of hippocampal pyramidal cells in vivo: activity-dependent phase-precession of action potentials. Hippocampus 8, 244–261 (1998).
    Article CAS Google Scholar
  22. 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).
    Article CAS Google Scholar
  23. Harris, K.D. et al. Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature 417, 738–741 (2002).
    Article CAS Google Scholar
  24. Losonczy, A., Zemelman, B.V., Vaziri, A. & Magee, J.C. Network mechanisms of theta related neuronal activity in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 13, 967–972 (2010).
    Article CAS Google Scholar
  25. Magee, J.C. Dendritic mechanisms of phase precession in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 86, 528–532 (2001).
    Article CAS Google Scholar
  26. Harvey, C.D., Collman, F., Dombeck, D.A. & Tank, D.W. Intracellular dynamics of hippocampal place cells during virtual navigation. Nature 461, 941–946 (2009).
    Article CAS Google Scholar
  27. Hangya, B., Li, Y., Muller, R.U. & Czurkó, A. Complementary spatial firing in place cell-interneuron pairs. J. Physiol. (Lond.) 588, 4165–4175 (2010).
    Article CAS Google Scholar
  28. Geisler, C., Robbe, D., Zugaro, M., Sirota, A. & Buzsáki, G. Hippocampal place cell assemblies are speed-controlled oscillators. Proc. Natl. Acad. Sci. USA 104, 8149–8154 (2007).
    Article CAS Google Scholar
  29. Maurer, A.P., Cowen, S.L., Burke, S.N., Barnes, C.A. & McNaughton, B.L. Phase precession in hippocampal interneurons showing strong functional coupling to individual pyramidal cells. J. Neurosci. 26, 13485–13492 (2006).
    Article CAS Google Scholar
  30. Hirase, H., Czurkó, A., Csicsvari, J. & Buzsáki, G. Firing rate and theta-phase coding by hippocampal pyramidal neurons during 'space clamping'. Eur. J. Neurosci. 11, 4373–4380 (1999).
    Article CAS Google Scholar
  31. Royer, S. et al. Multi-array silicon probes with integrated optical fibers: light-assisted perturbation and recording of local neural circuits in the behaving animal. Eur. J. Neurosci. 31, 2279–2291 (2010).
    Article Google Scholar
  32. O'Connor, D.H., Huber, D. & Svoboda, K. Reverse engineering the mouse brain. Nature 461, 923–929 (2009).
    Article CAS Google Scholar
  33. Buzsáki, G. et al. Hippocampal network patterns of activity in the mouse. Neuroscience 116, 201–211 (2003).
    Article Google Scholar
  34. Olton, D.S., Becker, J.T. & Handelmann, G.E. Hippocampus, space and memory. Behav. Brain Sci. 2, 313–322 (1979).
    Article Google Scholar
  35. Mizuseki, K., Sirota, A., Pastalkova, E. & Buzsáki, G. Theta oscillations provide temporal windows for local circuit computation in the entorhinal-hippocampal loop. Neuron 64, 267–280 (2009).
    Article CAS Google Scholar
  36. Buzsáki, G., Penttonen, M., Nádasdy, Z. & Bragin, A. Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vivo. Proc. Natl. Acad. Sci. USA 93, 9921–9925 (1996).
    Article Google Scholar
  37. Miles, R., Tóth, K., Gulyás, A.I., Hájos, N. & Freund, T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16, 815–823 (1996).
    Article CAS Google Scholar
  38. Takahashi, H. & Magee, J.C. Pathway interactions and synaptic plasticity in the dendritic tuft regions of CA1 pyramidal neurons. Neuron 62, 102–111 (2009).
    Article CAS Google Scholar
  39. Azouz, R., Jensen, M.S. & Yaari, Y. Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J. Physiol. (Lond.) 492, 211–223 (1996).
    Article CAS Google Scholar
  40. Lovett-Barron, M. et al. Regulation of neuronal input output transformation by tunable dendritic inhibition. Nat. Neurosci. 15, 423–430 (2012).
    Article CAS Google Scholar
  41. Harris, K.D., Hirase, H., Leinekugel, X., Henze, D.A. & Buzsáki, G. Temporal interaction between single spikes and complex spike bursts in hippocampal pyramidal cells. Neuron 32, 141–149 (2001).
    Article CAS Google Scholar
  42. Royer, S., Sirota, A., Patel, J. & Buzsáki, G. Distinct representations and theta dynamics in dorsal and ventral hippocampus. J. Neurosci. 30, 1777–1787 (2010).
    Article CAS Google Scholar
  43. Pouille, F. & Scanziani, M. Routing of spike series by dynamic circuits in the hippocampus. Nature 429, 717–723 (2004).
    Article CAS Google Scholar
  44. Kullmann, D.M. & Lamsa, K.P. Long-term synaptic plasticity in hippocampal interneurons. Nat. Rev. Neurosci. 8, 687–699 (2007).
    Article CAS Google Scholar
  45. Lisman, J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 20, 38–43 (1997).
    Article CAS Google Scholar
  46. Vinogradova, O.S. Hippocampus as comparator: role of the two input and two output systems of the hippocampus in selection and registration of information. Hippocampus 11, 578–598 (2001).
    Article CAS Google Scholar
  47. Freund, T.F. Interneuron Diversity series: rhythm and mood in perisomatic inhibition. Trends Neurosci. 26, 489–495 (2003).
    Article CAS Google Scholar
  48. Dupret, D., O'Neill, J., Pleydell-Bouverie, B. & Csicsvari, J. The reorganization and reactivation of hippocampal maps predict spatial memory performance. Nat. Neurosci. 13, 995–1002 (2010).
    Article CAS Google Scholar
  49. Atasoy, D., Aponte, Y., Su, H.H. & Sternson, S.M.A. FLEX switch targets Channelrhodopsin-2 to multiple cell types for imaging and long-range circuit mapping. J. Neurosci. 28, 7025–7030 (2008).
    Article CAS Google Scholar
  50. Grieger, J.C., Choi, V.W. & Samulski, R.J. Production and characterization of adeno-associated viral vectors. Nat. Protoc. 1, 1412–1428 (2006).
    Article CAS Google Scholar
  51. Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
    Article Google Scholar
  52. Harris, K.D., Henze, D.A., Csicsvari, J., Hirase, H. & Buzsáki, G. Accuracy of tetrode spike separation as determined by simultaneous intracellular and extracellular measurements. J. Neurophysiol. 84, 401–414 (2000).
    Article CAS Google Scholar
  53. Sirota, A. et al. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60, 683–697 (2008).
    Article CAS Google Scholar
  54. Fisher, N.I. Statistical Analysis of Circular Data (Cambridge University Press, 1993).
  55. Csicsvari, J., Hirase, H., Czurko, A. & Buzsáki, G. Reliability and state dependence of pyramidal cell-interneuron synapses in the hippocampus: an ensemble approach in the behaving rat. Neuron 21, 179–189 (1998).
    Article CAS Google Scholar
  56. Fujisawa, S., Amarasingham, A., Harrison, M.T. & Buzsáki, G. Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat. Neurosci. 11, 823–833 (2008).
    Article CAS Google Scholar
  57. Barthó, P. et al. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J. Neurophysiol. 92, 600–608 (2004).
    Article Google Scholar

Download references