Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest: Implications for age-related behavioral slowing

Nathan Insel, Lilian A. Patron, Lan T. Hoang, Saman Nematollahi, Lesley A. Schimanski, Peter Lipa, Carol A Barnes

Research output: Contribution to journalArticle

19 Citations (Scopus)

Abstract

Age-related cognitive and behavioral slowing may be caused by changes in the speed of neural signaling or by changes in the number of signaling steps necessary to achieve a given function. In the mammalian cortex, neural communication is organized by a 30-100 Hz "gamma" oscillation. There is a putative link between the gamma frequency and the speed of processing in a neural network: the dynamics of pyramidal neuron membrane time constants suggest that synaptic integration is framed by the gamma cycle, and pharmacological slowing of gamma also slows reaction times on behavioral tasks. The present experiments identify reductions in a robust 40-70 Hz gamma oscillation in the aged rat medial frontal cortex. The reductions were observed in the form of local field potentials, later peaks in fast-spiking neuron autocorrelations, and delays in the spiking of inhibitory neurons following local excitatory signals. Gamma frequency did not vary with movement speed, but rats with slower gamma also moved more slowly. Gamma frequency age differences were not observed in hippocampus. Hippocampal CA1 fast-spiking neurons exhibited interspike intervals consistent with a fast (70-100 Hz) gamma frequency, a pattern maintained across theta phases and theta frequencies independent of fluctuations in the average firing rates of the neurons. We propose that an average lengthening of the cortical 15-25 ms gamma cycle is one factor contributing to age-related slowing and that future attempts to offset cognitive declines will find a target in the response of fast-spiking inhibitory neurons to excitatory inputs.

Original languageEnglish (US)
Pages (from-to)16331-16344
Number of pages14
JournalJournal of Neuroscience
Volume32
Issue number46
DOIs
StatePublished - Nov 14 2012

Fingerprint

Frontal Lobe
Neurons
Pyramidal Cells
Hippocampus
Communication
Pharmacology
Membranes

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest : Implications for age-related behavioral slowing. / Insel, Nathan; Patron, Lilian A.; Hoang, Lan T.; Nematollahi, Saman; Schimanski, Lesley A.; Lipa, Peter; Barnes, Carol A.

In: Journal of Neuroscience, Vol. 32, No. 46, 14.11.2012, p. 16331-16344.

Research output: Contribution to journalArticle

Insel, Nathan ; Patron, Lilian A. ; Hoang, Lan T. ; Nematollahi, Saman ; Schimanski, Lesley A. ; Lipa, Peter ; Barnes, Carol A. / Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest : Implications for age-related behavioral slowing. In: Journal of Neuroscience. 2012 ; Vol. 32, No. 46. pp. 16331-16344.
@article{ff118b78f330476e979d951943c3a7d2,
title = "Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest: Implications for age-related behavioral slowing",
abstract = "Age-related cognitive and behavioral slowing may be caused by changes in the speed of neural signaling or by changes in the number of signaling steps necessary to achieve a given function. In the mammalian cortex, neural communication is organized by a 30-100 Hz {"}gamma{"} oscillation. There is a putative link between the gamma frequency and the speed of processing in a neural network: the dynamics of pyramidal neuron membrane time constants suggest that synaptic integration is framed by the gamma cycle, and pharmacological slowing of gamma also slows reaction times on behavioral tasks. The present experiments identify reductions in a robust 40-70 Hz gamma oscillation in the aged rat medial frontal cortex. The reductions were observed in the form of local field potentials, later peaks in fast-spiking neuron autocorrelations, and delays in the spiking of inhibitory neurons following local excitatory signals. Gamma frequency did not vary with movement speed, but rats with slower gamma also moved more slowly. Gamma frequency age differences were not observed in hippocampus. Hippocampal CA1 fast-spiking neurons exhibited interspike intervals consistent with a fast (70-100 Hz) gamma frequency, a pattern maintained across theta phases and theta frequencies independent of fluctuations in the average firing rates of the neurons. We propose that an average lengthening of the cortical 15-25 ms gamma cycle is one factor contributing to age-related slowing and that future attempts to offset cognitive declines will find a target in the response of fast-spiking inhibitory neurons to excitatory inputs.",
author = "Nathan Insel and Patron, {Lilian A.} and Hoang, {Lan T.} and Saman Nematollahi and Schimanski, {Lesley A.} and Peter Lipa and Barnes, {Carol A}",
year = "2012",
month = "11",
day = "14",
doi = "10.1523/JNEUROSCI.1577-12.2012",
language = "English (US)",
volume = "32",
pages = "16331--16344",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "46",

}

TY - JOUR

T1 - Reduced gamma frequency in the medial frontal cortex of aged rats during behavior and rest

T2 - Implications for age-related behavioral slowing

AU - Insel, Nathan

AU - Patron, Lilian A.

AU - Hoang, Lan T.

AU - Nematollahi, Saman

AU - Schimanski, Lesley A.

AU - Lipa, Peter

AU - Barnes, Carol A

PY - 2012/11/14

Y1 - 2012/11/14

N2 - Age-related cognitive and behavioral slowing may be caused by changes in the speed of neural signaling or by changes in the number of signaling steps necessary to achieve a given function. In the mammalian cortex, neural communication is organized by a 30-100 Hz "gamma" oscillation. There is a putative link between the gamma frequency and the speed of processing in a neural network: the dynamics of pyramidal neuron membrane time constants suggest that synaptic integration is framed by the gamma cycle, and pharmacological slowing of gamma also slows reaction times on behavioral tasks. The present experiments identify reductions in a robust 40-70 Hz gamma oscillation in the aged rat medial frontal cortex. The reductions were observed in the form of local field potentials, later peaks in fast-spiking neuron autocorrelations, and delays in the spiking of inhibitory neurons following local excitatory signals. Gamma frequency did not vary with movement speed, but rats with slower gamma also moved more slowly. Gamma frequency age differences were not observed in hippocampus. Hippocampal CA1 fast-spiking neurons exhibited interspike intervals consistent with a fast (70-100 Hz) gamma frequency, a pattern maintained across theta phases and theta frequencies independent of fluctuations in the average firing rates of the neurons. We propose that an average lengthening of the cortical 15-25 ms gamma cycle is one factor contributing to age-related slowing and that future attempts to offset cognitive declines will find a target in the response of fast-spiking inhibitory neurons to excitatory inputs.

AB - Age-related cognitive and behavioral slowing may be caused by changes in the speed of neural signaling or by changes in the number of signaling steps necessary to achieve a given function. In the mammalian cortex, neural communication is organized by a 30-100 Hz "gamma" oscillation. There is a putative link between the gamma frequency and the speed of processing in a neural network: the dynamics of pyramidal neuron membrane time constants suggest that synaptic integration is framed by the gamma cycle, and pharmacological slowing of gamma also slows reaction times on behavioral tasks. The present experiments identify reductions in a robust 40-70 Hz gamma oscillation in the aged rat medial frontal cortex. The reductions were observed in the form of local field potentials, later peaks in fast-spiking neuron autocorrelations, and delays in the spiking of inhibitory neurons following local excitatory signals. Gamma frequency did not vary with movement speed, but rats with slower gamma also moved more slowly. Gamma frequency age differences were not observed in hippocampus. Hippocampal CA1 fast-spiking neurons exhibited interspike intervals consistent with a fast (70-100 Hz) gamma frequency, a pattern maintained across theta phases and theta frequencies independent of fluctuations in the average firing rates of the neurons. We propose that an average lengthening of the cortical 15-25 ms gamma cycle is one factor contributing to age-related slowing and that future attempts to offset cognitive declines will find a target in the response of fast-spiking inhibitory neurons to excitatory inputs.

UR - http://www.scopus.com/inward/record.url?scp=84869026998&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84869026998&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.1577-12.2012

DO - 10.1523/JNEUROSCI.1577-12.2012

M3 - Article

C2 - 23152616

AN - SCOPUS:84869026998

VL - 32

SP - 16331

EP - 16344

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 46

ER -