Age Differences in Hippocampal Neural Timescales During Movie-Viewing

Abstract Episodic memory requires integrating information across multiple scales, a process theorized to be supported by a gradient of neural timescales along the anterior-posterior axis of the hippocampus that enables both coarse-and fine-grained representations. Aging is associated with changes in hippocampal function and declines in fine-grained episodic memory, but whether this impacts the gradient organization of the hippocampus is unknown. Additionally, the relationship between the neural timescales of the hippocampus and memory specificity remains unclear. Here, we analyzed the length of timescales of individual voxels in the hippocampus during movie-viewing, along with subsequent recall data, in a sample of young and older participants. Younger adults showed the expected anterior-to-posterior timescale gradient, replicating prior work. In contrast, older adults exhibited a reversal of the expected gradient. Older adults’ recall was coarser and more gist-like than that of younger adults. In younger adults, longer neural timescales were associated with less specific, more gist-like recall; this was seen predominantly in the posterior-lateral hippocampus. In contrast, no relationship between neural timescales and recall were observed in older adults. An exploratory analysis revealed a similar relationship between neural timescales and memory specificity in cortical regions, in younger but not older adults. These findings suggest that aging alters the organization of neural activity throughout the hippocampus and that neural timescales in the hippocampus and cortex are related to the specificity of memory. Significance statement As people age, episodic memories become more gist-like and less detailed. The hippocampus, which supports both gist and detailed memory, exhibits a neural timescale gradient—from slow-changing activity (longer timescales) to fast-changing activity (shorter timescales). This organization is theorized to support coarse-and fine-grained memory, respectively, yet a direct link to the age-related shift towards gist-like memory remains unestablished. Here, we identify an age-related shift in the hippocampal timescale gradient that parallels a decline in memory specificity. Furthermore, longer timescales in the hippocampus and cortical regions correlated with decreased memory specificity in younger adults. These findings demonstrate that aging is associated with a reorganization of hippocampal activity and that cortical timescales during encoding may relate to the specificity of memory. Competing Interest Statement The authors have declared no competing interest. Footnotes Conflict of Interest Statement: The authors declare no competing financial interests. Funding: This research was supported by the National Institutes of Health Grant R01AG031150 awarded to J.M.Z. and the National Institute on Aging Grant 1R03AG063224-01 awarded Z. M. R. N.R.B. and A.I.D. were supported by the National Institute on Aging Training Grant awarded to Dr. Jeffrey M. Zacks and Denise Head at Washington University in St. Louis (T32AG000030-47). A.I.D. was also supported by Grant GR0028512, National Science Foundation Graduate Research Fellowship Program Grant DGE-2139839 and Grant DGE-1745038. A.B.K. was supported by NINDS T32NS115672.