EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus

William E. Skaggs, Bruce L. McNaughton, Michele Permenter, Matthew Archibeque, Julie Vogt, David G Amaral, Carol A. Barnes

Research output: Contribution to journalArticle

84 Citations (Scopus)

Abstract

Neural unit activity and EEGs were recorded from inferior temporal regions of three rhesus macaques chronically implanted with "hyperdrives" holding 12 individually movable tetrodes. Recordings were made from each monkey over a period of ∼3 mo, while the electrodes were moved by small increments through the hippocampus and neighboring structures. After recording, the monkeys were necropsied, and the brains were sectioned and Nissl-stained, permitting identification of individual electrode tracks. The results establish that hippocampal pyramidal cells are "complex spike cells," firing at overall average rates of ∼0.3 Hz, with spike trains consisting of long periods of silence interspersed with bursts of activity. The results also establish that the monkey hippocampal EEG shows "sharp wave" events consisting of a high-frequency "ripple" oscillation (∼110 Hz) together with a large slow-wave EEG deflection lasting several hundred milliseconds. The evidence suggests that monkey sharp waves are probably generated mainly in the CA1 region and that sharp waves are associated with an inactive/drowsy-or-sleeping behavioral state, which is also associated with increased hippocampal pyramidal cell activity and increased hippocampal EEG amplitude. The results of this initial study of ensembles of primate hippocampal neurons are consistent with previous studies in rodents and consistent with the hypothesis that theories and models of hippocampal memory function developed on the basis of rat data may be applicable to a wide range of mammalian species.

Original languageEnglish (US)
Pages (from-to)898-910
Number of pages13
JournalJournal of Neurophysiology
Volume98
Issue number2
DOIs
StatePublished - Aug 2007

Fingerprint

Macaca
Haplorhini
Electroencephalography
Hippocampus
Pyramidal Cells
Electrodes
Temporal Lobe
Macaca mulatta
Primates
Rodentia
Neurons
Brain

ASJC Scopus subject areas

  • Physiology
  • Neuroscience(all)

Cite this

Skaggs, W. E., McNaughton, B. L., Permenter, M., Archibeque, M., Vogt, J., Amaral, D. G., & Barnes, C. A. (2007). EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. Journal of Neurophysiology, 98(2), 898-910. https://doi.org/10.1152/jn.00401.2007

EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. / Skaggs, William E.; McNaughton, Bruce L.; Permenter, Michele; Archibeque, Matthew; Vogt, Julie; Amaral, David G; Barnes, Carol A.

In: Journal of Neurophysiology, Vol. 98, No. 2, 08.2007, p. 898-910.

Research output: Contribution to journalArticle

Skaggs, WE, McNaughton, BL, Permenter, M, Archibeque, M, Vogt, J, Amaral, DG & Barnes, CA 2007, 'EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus', Journal of Neurophysiology, vol. 98, no. 2, pp. 898-910. https://doi.org/10.1152/jn.00401.2007
Skaggs, William E. ; McNaughton, Bruce L. ; Permenter, Michele ; Archibeque, Matthew ; Vogt, Julie ; Amaral, David G ; Barnes, Carol A. / EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus. In: Journal of Neurophysiology. 2007 ; Vol. 98, No. 2. pp. 898-910.
@article{773418e963a040a4b0903c181c74d058,
title = "EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus",
abstract = "Neural unit activity and EEGs were recorded from inferior temporal regions of three rhesus macaques chronically implanted with {"}hyperdrives{"} holding 12 individually movable tetrodes. Recordings were made from each monkey over a period of ∼3 mo, while the electrodes were moved by small increments through the hippocampus and neighboring structures. After recording, the monkeys were necropsied, and the brains were sectioned and Nissl-stained, permitting identification of individual electrode tracks. The results establish that hippocampal pyramidal cells are {"}complex spike cells,{"} firing at overall average rates of ∼0.3 Hz, with spike trains consisting of long periods of silence interspersed with bursts of activity. The results also establish that the monkey hippocampal EEG shows {"}sharp wave{"} events consisting of a high-frequency {"}ripple{"} oscillation (∼110 Hz) together with a large slow-wave EEG deflection lasting several hundred milliseconds. The evidence suggests that monkey sharp waves are probably generated mainly in the CA1 region and that sharp waves are associated with an inactive/drowsy-or-sleeping behavioral state, which is also associated with increased hippocampal pyramidal cell activity and increased hippocampal EEG amplitude. The results of this initial study of ensembles of primate hippocampal neurons are consistent with previous studies in rodents and consistent with the hypothesis that theories and models of hippocampal memory function developed on the basis of rat data may be applicable to a wide range of mammalian species.",
author = "Skaggs, {William E.} and McNaughton, {Bruce L.} and Michele Permenter and Matthew Archibeque and Julie Vogt and Amaral, {David G} and Barnes, {Carol A.}",
year = "2007",
month = "8",
doi = "10.1152/jn.00401.2007",
language = "English (US)",
volume = "98",
pages = "898--910",
journal = "Journal of Neurophysiology",
issn = "0022-3077",
publisher = "American Physiological Society",
number = "2",

}

TY - JOUR

T1 - EEG sharp waves and sparse ensemble unit activity in the macaque hippocampus

AU - Skaggs, William E.

AU - McNaughton, Bruce L.

AU - Permenter, Michele

AU - Archibeque, Matthew

AU - Vogt, Julie

AU - Amaral, David G

AU - Barnes, Carol A.

PY - 2007/8

Y1 - 2007/8

N2 - Neural unit activity and EEGs were recorded from inferior temporal regions of three rhesus macaques chronically implanted with "hyperdrives" holding 12 individually movable tetrodes. Recordings were made from each monkey over a period of ∼3 mo, while the electrodes were moved by small increments through the hippocampus and neighboring structures. After recording, the monkeys were necropsied, and the brains were sectioned and Nissl-stained, permitting identification of individual electrode tracks. The results establish that hippocampal pyramidal cells are "complex spike cells," firing at overall average rates of ∼0.3 Hz, with spike trains consisting of long periods of silence interspersed with bursts of activity. The results also establish that the monkey hippocampal EEG shows "sharp wave" events consisting of a high-frequency "ripple" oscillation (∼110 Hz) together with a large slow-wave EEG deflection lasting several hundred milliseconds. The evidence suggests that monkey sharp waves are probably generated mainly in the CA1 region and that sharp waves are associated with an inactive/drowsy-or-sleeping behavioral state, which is also associated with increased hippocampal pyramidal cell activity and increased hippocampal EEG amplitude. The results of this initial study of ensembles of primate hippocampal neurons are consistent with previous studies in rodents and consistent with the hypothesis that theories and models of hippocampal memory function developed on the basis of rat data may be applicable to a wide range of mammalian species.

AB - Neural unit activity and EEGs were recorded from inferior temporal regions of three rhesus macaques chronically implanted with "hyperdrives" holding 12 individually movable tetrodes. Recordings were made from each monkey over a period of ∼3 mo, while the electrodes were moved by small increments through the hippocampus and neighboring structures. After recording, the monkeys were necropsied, and the brains were sectioned and Nissl-stained, permitting identification of individual electrode tracks. The results establish that hippocampal pyramidal cells are "complex spike cells," firing at overall average rates of ∼0.3 Hz, with spike trains consisting of long periods of silence interspersed with bursts of activity. The results also establish that the monkey hippocampal EEG shows "sharp wave" events consisting of a high-frequency "ripple" oscillation (∼110 Hz) together with a large slow-wave EEG deflection lasting several hundred milliseconds. The evidence suggests that monkey sharp waves are probably generated mainly in the CA1 region and that sharp waves are associated with an inactive/drowsy-or-sleeping behavioral state, which is also associated with increased hippocampal pyramidal cell activity and increased hippocampal EEG amplitude. The results of this initial study of ensembles of primate hippocampal neurons are consistent with previous studies in rodents and consistent with the hypothesis that theories and models of hippocampal memory function developed on the basis of rat data may be applicable to a wide range of mammalian species.

UR - http://www.scopus.com/inward/record.url?scp=34547753014&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=34547753014&partnerID=8YFLogxK

U2 - 10.1152/jn.00401.2007

DO - 10.1152/jn.00401.2007

M3 - Article

C2 - 17522177

AN - SCOPUS:34547753014

VL - 98

SP - 898

EP - 910

JO - Journal of Neurophysiology

JF - Journal of Neurophysiology

SN - 0022-3077

IS - 2

ER -