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PMID: 11080262 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Distinct frequency preferences of different types of rat hippocampal neurones in response to oscillatory input currents.

The Journal of physiology ·Vol. 529 Pt 1 ·2000-11-15 ·Pages 205-13

Pike FG, Goddard RS, Suckling JM, Ganter P, Kasthuri N, Paulsen O

Abstract

1. Coherent network oscillations in several distinct frequency bands are seen in the hippocampus of behaving animals. To investigate how different neuronal types within this network respond to oscillatory inputs we made whole-cell current clamp recordings from three different types of neurones in the CA1 region of rat hippocampal slices: pyramidal cells, fast-spiking interneurones and horizontal interneurones, and recorded their response to sinusoidal inputs at physiologically relevant frequencies (1-100 Hz). 2. Pyramidal neurones showed firing preference to inputs at theta frequencies (range 2-7 Hz; n = 30). They showed subthreshold resonance in the same frequency range (2-7 Hz; mean 4.1 +/- 0.4 Hz; n = 19). 3. Interneurones differed in their firing properties. Horizontal interneurones in the stratum oriens showed firing preference to inputs at theta frequencies (range 1.5-10 Hz; n = 10). These interneurones also showed resonance at low frequencies (range 1-5 Hz; mean 2.4 +/- 0.5 Hz; n = 7). In contrast, fast-spiking interneurones with cell bodies in the pyramidal cell layer fired preferentially at input frequencies in the gamma band (range 30-50 Hz; n = 10/12). These interneurones showed resonance at beta-gamma frequencies (10-50 Hz; mean 26 +/- 5 Hz; n = 7/8). 4. Thus, in the hippocampus, different types of neurones have distinct frequency preferences. Therefore, in the CA1 layer of the hippocampal network, a compound oscillatory input may be segregated into distinct frequency components which are processed locally by distinct types of neurones.

MeSH Terms
Action Potentials/drug effects,physiology Algorithms Animals Electric Stimulation Electrophysiology Female Hippocampus/cytology,drug effects,physiology In Vitro Techniques Interneurons/drug effects,physiology Male Nerve Net/drug effects,physiology Neurons/drug effects,physiology Patch-Clamp Techniques Pyramidal Cells/drug effects,physiology Rats Rats, Wistar Tetrodotoxin/pharmacology
Chemicals
Tetrodotoxin
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Pike F G
Departments of Physiology and Pharmacology, and MRC Anatomical Neuropharmacology Unit, Oxford, UK. fgmaggs@doctors.org.uk
Goddard R S
Suckling J M
Ganter P
Kasthuri N
Paulsen O
References (28)
28 references, click to expand
  1. Resonance, oscillation and the intrinsic frequency preferences of neurons.
    Trends Neurosci. 2000 May;23(5):216-22 PMID: 10782127
  2. Human theta oscillations exhibit task dependence during virtual maze navigation.
    Nature. 1999 Jun 24;399(6738):781-4 PMID: 10391243
  3. Cellular bases of hippocampal EEG in the behaving rat.
    Brain Res. 1983 Oct;287(2):139-71 PMID: 6357356
  4. Intracellular records of theta rhythm in hippocampal CA1 cells of the rat.
    Brain Res. 1986 Mar 5;367(1-2):323-7 PMID: 3008923
  5. Quantification of membrane properties of trigeminal root ganglion neurons in guinea pigs.
    J Neurophysiol. 1986 May;55(5):995-1016 PMID: 3711977
  6. Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices.
    J Physiol. 1989 Oct;417:197-212 PMID: 2621591
  7. In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):897-901 PMID: 1992481
  8. Intrinsic membrane potential oscillations in hippocampal neurons in vitro.
    Brain Res. 1991 Jul 12;553(2):261-74 PMID: 1718544
  9. Synchronization of cortical activity and its putative role in information processing and learning.
    Annu Rev Physiol. 1993;55:349-74 PMID: 8466179
  10. Low- and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia.
    J Neurophysiol. 1993 Jul;70(1):97-116 PMID: 8395591
  11. Thalamocortical oscillations in the sleeping and aroused brain.
    Science. 1993 Oct 29;262(5134):679-85 PMID: 8235588
  12. Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites.
    Nature. 1994 Apr 28;368(6474):823-8 PMID: 8159242
  13. Resonant behavior and frequency preferences of thalamic neurons.
    J Neurophysiol. 1994 Feb;71(2):575-82 PMID: 8176426
  14. Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat.
    J Neurosci. 1995 Jan;15(1 Pt 1):47-60 PMID: 7823151
  15. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation.
    Nature. 1995 Feb 16;373(6515):612-5 PMID: 7854418
  16. Storage of 7 +/- 2 short-term memories in oscillatory subcycles.
    Science. 1995 Mar 10;267(5203):1512-5 PMID: 7878473
  17. Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modelling.
    J Physiol. 1995 Mar 15;483 ( Pt 3):621-40 PMID: 7776248
  18. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons.
    Nature. 1995 Nov 2;378(6552):75-8 PMID: 7477292
  19. Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation.
    Eur J Neurosci. 1995 Oct 1;7(10):2170-80 PMID: 8542073
  20. A mechanism for generation of long-range synchronous fast oscillations in the cortex.
    Nature. 1996 Oct 17;383(6601):621-4 PMID: 8857537
  21. Subthreshold membrane resonance in neocortical neurons.
    J Neurophysiol. 1996 Aug;76(2):683-97 PMID: 8871191
  22. Interneurons of the hippocampus.
    Hippocampus. 1996;6(4):347-470 PMID: 8915675
  23. Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus.
    J Physiol. 1998 Feb 15;507 ( Pt 1):185-99 PMID: 9490837
  24. Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection.
    J Neurophysiol. 1998 Mar;79(3):1592-6 PMID: 9497437
  25. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro.
    Nature. 1998 Jul 9;394(6689):186-9 PMID: 9671302
  26. Intrinsic theta-frequency membrane potential oscillations in hippocampal CA1 interneurons of stratum lacunosum-moleculare.
    J Neurophysiol. 1999 Mar;81(3):1296-307 PMID: 10085356
  27. Activation of nicotinic acetylcholine receptors patterns network activity in the rodent hippocampus.
    J Physiol. 1999 Jul 1;518 ( Pt 1):131-40 PMID: 10373695
  28. Cholinergic induction of oscillations in the hippocampal slice in the slow (0.5-2 Hz), theta (5-12 Hz), and gamma (35-70 Hz) bands.
    Hippocampus. 2000;10(2):187-97 PMID: 10791841
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
2000-11-15
Pages
205-13
Language
English
Region
England
NLM ID
0266262
PMCID
PMC2270176
Subset
IM
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