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Aged Rats Exhibit Altered Behavior-Induced Oscillatory Activity, Place Cell Firing Rates, and Spatial Information Content in the CA1 Region of the Hippocampus
Journal of Neuroscience ( IF 5.3 ) Pub Date : 2022-06-01 , DOI: 10.1523/jneurosci.1855-21.2022
Lindsey M. Crown , Daniel T. Gray , Lesley A. Schimanski , Carol A. Barnes , Stephen L. Cowen

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.

SIGNIFICANCE STATEMENT 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.



中文翻译:

老年大鼠在海马 CA1 区域表现出改变的行为诱导的振荡活动、位置细胞放电率和空间信息内容

海马 gamma 和 theta 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 gamma 和 theta 频率,尽管尚未很好地研究年龄如何改变这种调节。在这里,我们检查 gamma 和 theta 局部场电位,并在年轻和老年雄性大鼠的海马 CA1 区域中放置细胞活动,因为它们在 31 天内执行空间眨眼调节任务。尽管两组的平均伽马频率相似,但在老年动物中,伽马频率随着跑步速度的增加而增加,速度较慢。相比之下,theta 频率在两组中随速度的变化相似,但在老年动物的速度上较低。尽管这些频率与减速和速度的比例相同,但在两个年龄组中,加速度与伽马频率的相关性较低。此外,在较年长的动物中,峰值锁相到伽马而非 theta 的情况更大。最后,老年大鼠的场内发射率降低,但场内每个尖峰的空间信息更多。这些数据支持运动行为和局部场电位活动之间的密切关系,并表明年龄显着影响这种关系。此外,观察到的 CA1 位置细胞放电率和信息内容的变化支持了这样一个假设,即年龄可能导致更一般和上下文不变的海马表示对更详细的信息。

重要性声明海马振荡和位置细胞活动对主动运动产生的感觉运动输入很敏感,但对老年海马功能的研究通常不能解释这一点。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缩放与速度、尖峰场相干性、空间信息内容和 CA1 位置细胞的场内发射率的差异。这些结果表明,年龄对运动和海马振荡活动之间的关系有影响,这可能表明传入输入的改变。这些数据还支持这样的假设,即与年轻的海马位置细胞相比,老化的海马位置细胞可能更常代表更一般的空间信息。如果真实,

更新日期:2022-06-02
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