4.7 Article

Aged Rats Exhibit Altered Behavior-Induced Oscillatory Activity, Place Cell Firing Rates, and Spatial Information Content in the CA1 Region of the Hippocampus

Journal

JOURNAL OF NEUROSCIENCE
Volume 42, Issue 22, Pages 4505-4516

Publisher

SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1855-21.2022

Keywords

cross-frequency coupling; gamma; hippocampus; oscillation; place cell; theta

Categories

Funding

  1. Evelyn F. McKnight Brain Research Foundation
  2. National Institutes of Health [AG012609]
  3. Canadian Institutes of Health Research Grant [SIB78537]
  4. Alberta Heritage Foundation for Medical Research Grant [20060436]

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This study investigates the effects of locomotor activity and age on gamma and theta frequencies in the hippocampus of rats. The results show that age affects the modulation of gamma and theta frequencies, with older rats showing slower increases in gamma frequency and lower theta frequencies. Acceleration is also found to have a lower correlation with gamma frequency in both age groups. Older animals have greater spike phase-locking to gamma and reduced firing rates within place fields, but higher spatial information content per spike. These findings suggest that locomotor behavior and age significantly impact local-field potential activity in the hippocampus.
Hippocampal gamma and theta oscillations are associated with mnemonic and navigational processes and adapt to changes in the behavioral state of an animal to optimize spatial information processing. It has been shown that locomotor activity modulates gamma and theta frequencies in rats, although how age alters this modulation has not been well studied. Here, we examine gamma and theta local-field potential and place cell activity in the hippocampus CA1 region of young and old male rats as they performed a spatial eye-blink conditioning task across 31 d. Although mean gamma frequency was similar in both groups, gamma frequency increased with running speed at a slower rate in old animals. By contrast, theta frequencies scaled with speed similarly in both groups but were lower across speeds in old animals. Although these frequencies scaled equally well with deceleration and speed, acceleration was less correlated with gamma frequency in both age groups. Additionally, spike phase-locking to gamma, but not theta, was greater in older animals. Finally, aged rats had reduced within-field firing rates but greater spatial information per spike within the field. These data support a strong relationship between locomotor behavior and local-field potential activity and suggest that age significantly affects this relationship. Furthermore, observed changes in CA1 place cell firing rates and information content lend support to the hypothesis that age may result in more general and context-invariant hippocampal representations over more detailed information. These results may explain the observation that older adults tend to recall the gist of an experience rather than the details.

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