Contrasting patterns of receptive field plasticity in the hippocampus and the entorhinal cortex: an adaptive filtering approach.

Loren M Frank, Uri T Eden, Victor Solo, Matthew A Wilson, Emery N Brown
Author Information
  1. Loren M Frank: Neuroscience Statistics Research Laboratory, Department of Anesthesia and Critical Care, Massachusetts General Hospital and Harvard University/Massachusetts Institute of Technology, Boston, Massachusetts 02114, USA. loren@neurostat.mgh.harvard.edu

Abstract

Neural receptive fields are frequently plastic: a neural response to a stimulus can change over time as a result of experience. We developed an adaptive point process filtering algorithm that allowed us to estimate the dynamics of both the spatial receptive field (spatial intensity function) and the interspike interval structure (temporal intensity function) of neural spike trains on a millisecond time scale without binning over time or space. We applied this algorithm to both simulated data and recordings of putative excitatory neurons from the CA1 region of the hippocampus and the deep layers of the entorhinal cortex (EC) of awake, behaving rats. Our simulation results demonstrate that the algorithm accurately tracks simultaneous changes in the spatial and temporal structure of the spike train. When we applied the algorithm to experimental data, we found consistent patterns of plasticity in the spatial and temporal intensity functions of both CA1 and deep EC neurons. These patterns tended to be opposite in sign, in that the spatial intensity functions of CA1 neurons showed a consistent increase over time, whereas those of deep EC neurons tended to decrease, and the temporal intensity functions of CA1 neurons showed a consistent increase only in the "theta" (75-150 msec) region, whereas those of deep EC neurons decreased in the region between 20 and 75 msec. In addition, the minority of deep EC neurons whose spatial intensity functions increased in area over time fired in a significantly more spatially specific manner than non-increasing deep EC neurons. We hypothesize that this subset of deep EC neurons may receive more direct input from CA1 and may be part of a neural circuit that transmits information about the animal's location to the neocortex.

Keywords

References

  1. J Neurosci. 1997 Jul 1;17(13):5183-95 [PMID: 9185556]
  2. J Neurosci. 1994 Apr;14(4):2339-56 [PMID: 8158272]
  3. Behav Brain Res. 1997 Apr;85(1):71-92 [PMID: 9095343]
  4. Neural Comput. 2002 Feb;14(2):325-46 [PMID: 11802915]
  5. J Neurophysiol. 2001 Oct;86(4):2029-40 [PMID: 11600659]
  6. J Neurophysiol. 1997 Aug;78(2):1062-81 [PMID: 9307135]
  7. Proc Natl Acad Sci U S A. 1997 Aug 5;94(16):8918-21 [PMID: 9238078]
  8. Neuroscience. 1983 Nov;10(3):639-65 [PMID: 6646426]
  9. Science. 1991 Nov 29;254(5036):1377-9 [PMID: 1962197]
  10. Brain Res. 1986 Nov 29;398(2):242-52 [PMID: 3026567]
  11. Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):12261-6 [PMID: 11593043]
  12. Exp Brain Res. 1987;67(3):502-9 [PMID: 3653312]
  13. Prog Brain Res. 1990;83:287-300 [PMID: 2392566]
  14. Curr Opin Neurobiol. 1993 Aug;3(4):570-7 [PMID: 8219724]
  15. Brain Res. 1983 Oct;287(2):139-71 [PMID: 6357356]
  16. Prog Neurobiol. 1999 Feb;57(2):165-224 [PMID: 9987805]
  17. Eur J Neurosci. 1999 Oct;11(10):3715-24 [PMID: 10564378]
  18. J Neurosci. 1998 Jan 1;18(1):388-98 [PMID: 9412515]
  19. Eur J Neurosci. 1995 Apr 1;7(4):753-65 [PMID: 7620624]
  20. Behav Neurosci. 1999 Aug;113(4):643-62 [PMID: 10495074]
  21. J Neurophysiol. 1993 Jun;69(6):1918-29 [PMID: 8350131]
  22. J Neurosci. 1997 Sep 1;17(17):6769-82 [PMID: 9254688]
  23. J Neurosci. 1987 Jul;7(7):1935-50 [PMID: 3612225]
  24. Neuron. 2000 Jul;27(1):169-78 [PMID: 10939340]
  25. Brain Res. 1971 Nov;34(1):171-5 [PMID: 5124915]
  26. J Neurosci Methods. 2001 Jan 30;105(1):25-37 [PMID: 11166363]
  27. Neuron. 2001 Aug 30;31(4):631-8 [PMID: 11545721]
  28. Hippocampus. 1993 Jul;3(3):317-30 [PMID: 8353611]
  29. Science. 1994 Jan 28;263(5146):520-2 [PMID: 8290960]
  30. Exp Brain Res. 1983;52(1):41-9 [PMID: 6628596]
  31. Science. 1993 Aug 20;261(5124):1055-8 [PMID: 8351520]
  32. J Neurosci. 1994 Oct;14(10):6160-70 [PMID: 7931570]
  33. J Neurosci. 1998 Sep 15;18(18):7411-25 [PMID: 9736661]
  34. Neuropharmacology. 1998 Apr-May;37(4-5):657-76 [PMID: 9705004]
  35. Exp Brain Res. 1993;96(3):457-72 [PMID: 8299747]
  36. Neuron. 2000 Mar;25(3):707-15 [PMID: 10774737]
  37. Neural Comput. 2001 Aug;13(8):1713-20 [PMID: 11506667]
  38. Neuron. 1999 Apr;22(4):657-60 [PMID: 10230786]
  39. Science. 1992 May 15;256(5059):1025-7 [PMID: 1589772]

Grants

  1. K02 MH061637/NIMH NIH HHS
  2. R01 MH059733/NIMH NIH HHS
  3. MH59733/NIMH NIH HHS
  4. MH61637/NIMH NIH HHS

MeSH Term

Action Potentials
Algorithms
Animals
Computer Simulation
Electrodes, Implanted
Entorhinal Cortex
Hippocampus
Models, Neurological
Nerve Net
Neuronal Plasticity
Neurons
Pattern Recognition, Automated
Rats
Signal Processing, Computer-Assisted
Space Perception
Theta Rhythm
Wakefulness

Word Cloud

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