Distinguishing the precision of spatial recollection from its success: Evidence from healthy aging and unilateral mesial temporal lobe resection

Abstract

Successful episodic recollection can vary in the precision of the information recalled. The hypothesis that recollection precision requires functional neuroanatomical contributions distinct from those required for recollection success remains controversial. Some findings in individuals with hippocampal lesions have indicated that precision is dependent on the hippocampus. However, other neuroimaging and lesion studies have implicated regions outside of the mesial temporal lobe (MTL) in precision, such as parietal cortex. To further elucidate distinctions of recollection precision versus success, we examined whether they were differentially sensitive to aging and to unilateral MTL lesions. Precision and success were measured using a novel task that required memory for item-location associations across different spatial contexts. We found impairments in recollection precision, but not success, in older adults (59-80 years) relative to younger adults (18-33 years). Recollection precision was also selectively impaired in individuals with unilateral MTL resections made to treat refractory epilepsy. Moreover, recollection precision was significantly worse when resections included the hippocampus compared to when only non-hippocampal MTL tissue was resected. These findings suggest that the MTL is critically involved in the high-resolution binding required to support spatial recollection precision, and thus provide evidence for functional neuroanatomical differences between recollection success and precision.

Healthy ageing reduces the precision of episodic memory retrieval

“…The current findings of age-related degradation of the precision of episodic memory retrieval are consistent with previous accounts proposing a loss of quality, and specificity, of memory representations in older age (Burke et al, 2018;Goh, 2011;Li, Lindenberger, & Sikström, 2001;Trelle et al, 2017). The observed pattern of reduced precision with preserved retrieval success is in line with studies proposing that while memory for the gist of an event, or stimulus, might be preserved in ageing, the more fine-grained details tend to be lost (Dennis et al, 2007(Dennis et al, , 2008Kensinger & Schacter, 1999;Nilakantan et al, 2018). However, whereas previous experiments have predominantly relied on categorical measures of memory success, tasks that emphasise spatial features exclusively, or comparisons between tasks conditions to draw inferences about changes in memory quality, the current study provides a more direct and versatile behavioural measure of memory fidelity, separable from differences in the probability of successful retrieval.…”

“…This apparent discrepancy might be explained by age-related decreases on categorical measures of memory success in previous studies being partially attributable to reduced fidelity of the underlying memory representations, rather than a failure to retrieve the representations per se (Nilakantan et al, 2018). For instance, a failure to discriminate between two similar sources of memories, such between two female or two male voices (Simons et al, 2004), could result from a noisier memory representation of the source, leading to selection of the incorrect retrieval response, and thereby reduced retrieval success.…”

“…In working memory (WM) research, continuous report tasks, providing a more direct measure of memory fidelity, have been fruitful in elucidating the 6 specific components of short-term memory degradation in older age, revealing age-related decreases in mnemonic precision and increases in binding errors, whereas no age differences in the success of memory retrieval were detected (Peich, Husain, & Bays, 2013). This approach has recently been extended to investigate age-related changes in object-spatial location binding in long-term memory, suggesting that the precision of LTM retrieval might similarly be sensitive to age-related decline (Nilakantan, Bridge, VanHaerents, & Voss, 2018).…”

“…Previous research has implicated the retrieval of contextual information, such as spatial location, as particularly sensitive to age-related degradation (Chalfonte & Johnson, 1996;Kukolja, Thiel, Wilms, Mirzazade, & Fink, 2009;Nilakantan et al, 2018;Old & Naveh-Benjamin, 2008;Rajah, Languay, & Valiquette, 2010;Spencer & Raz, 1995), therefore in the 7 first experiment we used a location memory task to examine the effects of ageing on the success and precision of episodic memory retrieval. In contrast to memory for the context in which studied items were encountered, memory for the items themselves has typically been considered less vulnerable to age-related decline (Old & Naveh-Benjamin, 2008;Spencer & Raz, 1995).…”

Schematic memories develop quickly, but are not expressed unless necessary

“…This is different from much of the schema literature in two ways: (1) our measures of schema-consistency and memory precision are continuous, measured by each image's proximity to the central location of all images of the same category, and the distance between its encoded and retrieved location, respectively, and (2) participants needed to map prior knowledge of category membership onto new, trial-specific spatial information to learn a new schema about the locations of images. Past uses of continuous retrieval reports have enabled researchers to distinguish the precision of episodic memories from their overall retrieval success 38,39 , reveal subtle memory deficits in healthy aging and in patients with altered MTL function 40 , and map separate neural contributions to different aspects of memory retrieval, such as precision, confidence, and vividness 41,42 . In contrast, most research in schematic memory tends to discretize memoranda as schema-consistent or not, using prior knowledge that participants already know, like famous faces, word pairs that are semantically related word pairs, or dot patterns that resemble letters [43][44][45] , although there are numerous exceptions 11,16,17,31 .…”