Attenuated activity across multiple cell types and reduced monosynaptic connectivity in the aged perirhinal cortex

Andrew P. Maurer, Sara N. Burke, Kamran Diba, Carol A. Barnes

Research output: Research - peer-reviewArticle

Abstract

The perirhinal cortex (PER), which is critical for associative memory and stimulus discrimination, has been described as a wall of inhibition between the neocortex and hippocampus. With advanced age, rats show deficits on PER-dependent behavioral tasks and fewer PER principal neurons are activated by stimuli, but the role of PER interneurons in these altered circuit properties in old age has not been characterized. In the present study, PER neurons were recorded while rats traversed a circular track bidirectionally in which the track was either empty or contained eight novel objects evenly spaced around the track. Putative interneurons were discriminated from principal cells based on the autocorrelogram, waveform parameters, and firing rate. While object modulation of interneuron firing was observed in both young and aged rats, PER interneurons recorded from old animals had lower firing rates compared with those from young animals. This difference could not be accounted for by differences in running speed, as the firing rates of PER interneurons did not show significant velocity modulation. Finally, in the aged rats, relative to young rats, there was a significant reduction in detected excitatory and inhibitory monosynaptic connections. Together these data suggest that with advanced age there may be reduced afferent drive from excitatory cells onto interneurons that may compromise the wall of inhibition between the hippocampus and cortex. This circuit dysfunction could erode the function of temporal lobe networks and ultimately contribute to cognitive aging.

LanguageEnglish (US)
Pages8965-8974
Number of pages10
JournalJournal of Neuroscience
Volume37
Issue number37
DOIs
StatePublished - 2017

Fingerprint

Perirhinal Cortex
Interneurons
Hippocampus
Neurons
Inhibition (Psychology)
Neocortex
Temporal Lobe
Running
Drive
Cognitive Aging
Discrimination (Psychology)

Keywords

  • Hippocampus
  • Medial temporal lobe
  • Object field
  • Place field
  • Rat

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Attenuated activity across multiple cell types and reduced monosynaptic connectivity in the aged perirhinal cortex. / Maurer, Andrew P.; Burke, Sara N.; Diba, Kamran; Barnes, Carol A.

In: Journal of Neuroscience, Vol. 37, No. 37, 2017, p. 8965-8974.

Research output: Research - peer-reviewArticle

@article{a77dae58430042e1be734ea125827e1a,
title = "Attenuated activity across multiple cell types and reduced monosynaptic connectivity in the aged perirhinal cortex",
abstract = "The perirhinal cortex (PER), which is critical for associative memory and stimulus discrimination, has been described as a wall of inhibition between the neocortex and hippocampus. With advanced age, rats show deficits on PER-dependent behavioral tasks and fewer PER principal neurons are activated by stimuli, but the role of PER interneurons in these altered circuit properties in old age has not been characterized. In the present study, PER neurons were recorded while rats traversed a circular track bidirectionally in which the track was either empty or contained eight novel objects evenly spaced around the track. Putative interneurons were discriminated from principal cells based on the autocorrelogram, waveform parameters, and firing rate. While object modulation of interneuron firing was observed in both young and aged rats, PER interneurons recorded from old animals had lower firing rates compared with those from young animals. This difference could not be accounted for by differences in running speed, as the firing rates of PER interneurons did not show significant velocity modulation. Finally, in the aged rats, relative to young rats, there was a significant reduction in detected excitatory and inhibitory monosynaptic connections. Together these data suggest that with advanced age there may be reduced afferent drive from excitatory cells onto interneurons that may compromise the wall of inhibition between the hippocampus and cortex. This circuit dysfunction could erode the function of temporal lobe networks and ultimately contribute to cognitive aging.",
keywords = "Hippocampus, Medial temporal lobe, Object field, Place field, Rat",
author = "Maurer, {Andrew P.} and Burke, {Sara N.} and Kamran Diba and Barnes, {Carol A.}",
year = "2017",
doi = "10.1523/JNEUROSCI.0531-17.2017",
volume = "37",
pages = "8965--8974",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "37",

}

TY - JOUR

T1 - Attenuated activity across multiple cell types and reduced monosynaptic connectivity in the aged perirhinal cortex

AU - Maurer,Andrew P.

AU - Burke,Sara N.

AU - Diba,Kamran

AU - Barnes,Carol A.

PY - 2017

Y1 - 2017

N2 - The perirhinal cortex (PER), which is critical for associative memory and stimulus discrimination, has been described as a wall of inhibition between the neocortex and hippocampus. With advanced age, rats show deficits on PER-dependent behavioral tasks and fewer PER principal neurons are activated by stimuli, but the role of PER interneurons in these altered circuit properties in old age has not been characterized. In the present study, PER neurons were recorded while rats traversed a circular track bidirectionally in which the track was either empty or contained eight novel objects evenly spaced around the track. Putative interneurons were discriminated from principal cells based on the autocorrelogram, waveform parameters, and firing rate. While object modulation of interneuron firing was observed in both young and aged rats, PER interneurons recorded from old animals had lower firing rates compared with those from young animals. This difference could not be accounted for by differences in running speed, as the firing rates of PER interneurons did not show significant velocity modulation. Finally, in the aged rats, relative to young rats, there was a significant reduction in detected excitatory and inhibitory monosynaptic connections. Together these data suggest that with advanced age there may be reduced afferent drive from excitatory cells onto interneurons that may compromise the wall of inhibition between the hippocampus and cortex. This circuit dysfunction could erode the function of temporal lobe networks and ultimately contribute to cognitive aging.

AB - The perirhinal cortex (PER), which is critical for associative memory and stimulus discrimination, has been described as a wall of inhibition between the neocortex and hippocampus. With advanced age, rats show deficits on PER-dependent behavioral tasks and fewer PER principal neurons are activated by stimuli, but the role of PER interneurons in these altered circuit properties in old age has not been characterized. In the present study, PER neurons were recorded while rats traversed a circular track bidirectionally in which the track was either empty or contained eight novel objects evenly spaced around the track. Putative interneurons were discriminated from principal cells based on the autocorrelogram, waveform parameters, and firing rate. While object modulation of interneuron firing was observed in both young and aged rats, PER interneurons recorded from old animals had lower firing rates compared with those from young animals. This difference could not be accounted for by differences in running speed, as the firing rates of PER interneurons did not show significant velocity modulation. Finally, in the aged rats, relative to young rats, there was a significant reduction in detected excitatory and inhibitory monosynaptic connections. Together these data suggest that with advanced age there may be reduced afferent drive from excitatory cells onto interneurons that may compromise the wall of inhibition between the hippocampus and cortex. This circuit dysfunction could erode the function of temporal lobe networks and ultimately contribute to cognitive aging.

KW - Hippocampus

KW - Medial temporal lobe

KW - Object field

KW - Place field

KW - Rat

UR - http://www.scopus.com/inward/record.url?scp=85029469789&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85029469789&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.0531-17.2017

DO - 10.1523/JNEUROSCI.0531-17.2017

M3 - Article

VL - 37

SP - 8965

EP - 8974

JO - Journal of Neuroscience

T2 - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 37

ER -