Development and Decline of the Hippocampal Long-Axis Specialization and Differentiation During Encoding and Retrieval of Episodic Memories

Abstract

Change in hippocampal function is a major factor in life span development and decline of episodic memory. Evidence indicates a long-axis specialization where anterior hippocampus is more engaged during encoding than during retrieval, and posterior more engaged during retrieval than during encoding. We tested the life span trajectory of hippocampal long-axis episodic memory-related activity and functional connectivity (FC) in 496 participants (6.8–80.8 years) encoding and retrieving associative memories. We found evidence for a long-axis encoding–retrieval specialization that declined linearly during development and aging, eventually vanishing in the older adults. This was mainly driven by age effects on retrieval, which was associated with gradually lower activity from childhood to adulthood, followed by positive age relationships until 70 years. This pattern of age effects characterized task engagement regardless of memory success or failure. Especially for retrieval, children engaged posterior hippocampus more than anterior, while anterior was relatively more activated already in teenagers. Significant intrahippocampal connectivity was found during task, which declined with age. The results suggest that hippocampal long-axis differentiation and communication during episodic memory tasks develop rapidly during childhood, are different in older compared with younger adults, and that the age effects are related to task engagement, not the successful retrieval of episodic memories specifically.

Microstructural Integrity of the Hippocampus During Childhood: Relations With Age and Source Memory

“…The appearance of a stronger relations between hippocampal MD and source memory in posterior hippocampus aligns with work showing stronger recruitment of the posterior subregion during the retrieval of associative memories in children compared to teenagers and adults ( DeMaster et al, 2013 ; Langnes et al, 2019b ). Functional specialization of anterior versus posterior hippocampus is still debated (see Poppenk et al, 2013 , for review).…”

Intrinsic hippocampal functional connectivity underlying rigid memory in children and adolescents with autism spectrum disorder: A case–control study

“…The left anterior hippocampus (MNI coordinates of −28, −12, −20), left posterior hippocampus (−28, −24, −12), right anterior hippocampus (28, −12, −20), and right posterior hippocampus (32, −22, −12)-all with a 6 mm radius sphere-were defined as seed ROIs. The anterior-posterior hippocampal segmentation was consistent with another study examining memory-related activation in a wide age range (6.8-80.8 years) with MNI coordinates of y = −21 corresponding to the appearance of the uncus of the parahippocampal gyrus (Langnes et al, 2019). Pearson's correlations between the mean time course of each ROI and that of each voxel of whole brain were calculated at the single-subject level, and the correlation coefficients were transformed using a Fisher z-transformation.…”

“…TD children can use the hippocampal network for successful memory (Ngo et al, 2017;Ofen, 2012;Tang et al, 2018), and hippocampal maturation in the anterior-posterior axis may support successful memory (Demaster & Ghetti, 2013). Encoding-retrieval differentiation in the anterior-posterior axis of the hippocampus has been observed in children (Langnes et al, 2019). As such, altered neural connectivity of the hippocampus may provide information on atypical learning and memory in children with ASD.…”

Exercise Training-Related Changes in Cortical Gray Matter Diffusivity and Cognitive Function in Mild Cognitive Impairment and Healthy Older Adults

“…In the context of development, gray matter MD is generally negatively associated with age and better cognitive performance and is thought to represent increased myelination and axonal and neural density (Mah et al, 2017;Fjell et al, 2019;Callow et al, 2020). Meanwhile, in older adults, age and disease progression are usually positively associated with gray matter MD, which is believed to result from a general decline in dendritic and synaptic density (Ray et al, 2006;Pereira et al, 2014;Weston et al, 2015;Salminen et al, 2016;O'Shea et al, 2016;Langnes et al, 2019).…”