Evelyn F. McKnight Brain Institute, University of Arizona, Tucson, Arizona 85724.
Department of Psychology, University of Arizona, Tucson, Arizona 85721.
J Neurosci. 2022 Jun 1;42(22):4505-4516. doi: 10.1523/JNEUROSCI.1855-21.2022. Epub 2022 Apr 27.
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. Hippocampal oscillations and place cell activity are sensitive to sensorimotor input generated from active locomotion, yet studies of aged hippocampal function often do not account for this. By considering locomotion and spatial location, we identify novel age-associated differences in the scaling of oscillatory activity with speed, spike-field coherence, spatial information content, and within-field firing rates of CA1 place cells. These results indicate that age has an impact on the relationship between locomotion and hippocampal oscillatory activity, perhaps indicative of alterations to afferent input. These data also support the hypothesis that aged hippocampal place cells, compared with young, may more often represent more general spatial information. If true, these results may help explain why older humans tend to recall less specific and more gist-like information.
海马体的γ和θ振荡与记忆和导航过程相关，并适应动物行为状态的变化，以优化空间信息处理。已经表明，运动活动调节大鼠的γ和θ频率，尽管年龄如何改变这种调节尚未得到很好的研究。在这里，我们在年轻和老年雄性大鼠执行空间眨眼条件反射任务时，检查海马体 CA1 区域的γ和θ局部场电位和位置细胞活动，共 31 天。尽管两组的平均γ频率相似，但老年动物的γ频率随跑步速度的增加而增加的速度较慢。相比之下，两组的θ频率与速度相似，但在老年动物中速度较低。尽管这些频率与减速和速度同样良好地缩放，但在两个年龄组中，加速度与γ频率的相关性较小。此外，与θ相比，向γ的尖峰相位锁定在老年动物中更大。最后，老年大鼠的场内发射率降低，但场中每个尖峰的空间信息量增加。这些数据支持运动行为与局部场电位活动之间的强关系，并表明年龄对此关系有显著影响。此外，CA1 位置细胞放电率和信息量的观察变化支持以下假设：年龄可能导致海马体表示在更详细的信息上更通用和上下文不变。这些结果可以解释老年人倾向于回忆经验的要点而不是细节的观察结果。海马体振荡和位置细胞活动对来自主动运动的感觉运动输入敏感，然而，老年海马体功能的研究通常不考虑这一点。通过考虑运动和空间位置，我们确定了与年龄相关的新的振荡活动与速度、尖峰场相干性、空间信息量和 CA1 位置细胞场内发射率的缩放差异。这些结果表明，年龄对运动和海马体振荡活动之间的关系有影响，可能表明传入输入的改变。这些数据还支持以下假设：与年轻相比，年老的海马体位置细胞可能更经常代表更一般的空间信息。如果是这样，这些结果可能有助于解释为什么老年人往往回忆起不太具体和更要点式的信息。
