Neural correlates of retrieval-based memory enhancement: an fMRI study of the testing effect

Abstract

Restudying material is a common method for learning new information, but not necessarily an effective one. Research on the testing effect shows that practice involving retrieval from memory can facilitate later memory in contrast to passive restudy. Despite extensive behavioral work, the brain processes that make retrieval an effective learning strategy remain unclear. In the present experiment, we explored how initially retrieving items affected memory a day later as compared to a condition involving traditional restudy. In contrast to restudy, initial testing that contributed to future memory success was associated with engagement of several regions including the anterior hippocampus, lateral temporal cortices, and medial prefrontal cortex (PFC). Additionally, testing enhanced hippocampal connectivity with ventrolateral PFC and midline regions. These findings indicate that the testing effect may be contingent on processes that are typically thought to support memory success at encoding (e.g. relational binding, selection and elaboration of semantically-related information) in addition to those more often associated with retrieval (e.g. memory search).

Keywords: Episodic memory; Hippocampus; Medial PFC; Retrieval practice; Testing effect; fMRI.

© 2013 Elsevier Ltd. All rights reserved.

Figures

Figure 1

Schematic of one run from the fMRI portion of experiment. Each Study and Practice block contained 16 trials. Twenty-four hours after the scan session, memory for all initial word pairs was assessed in a final cued-recall test (not shown). Performance on this final test was used to backsort Practice (i.e. Test/Restudy) trials as either subsequently remembered or forgotten.

Figure 2

Behavioral testing effect. Single subject behavioral performance showing proportion correct recall during final cued-recall test as a function of scan-session practice condition (Test/Restudy).

Figure 3

Testing effect interaction. Brain regions showing a condition (Test/Restudy) by memory (subsequently remembered/subsequently forgotten) interaction. Interaction effects are evident in left middle/inferior temporal gyri (A) and bilateral anterior hippocampus (B, C). Bars reflect SME (difference in activity between subsequently remembered and forgotten). Error bars denote standard error.

Figure 4

Hippocampal connectivity interaction. Brain regions showing hippocampal connectivity differences by condition and subsequent memory. Regions in both posterior (posterior cingulate/precuneus, A) and anterior (medial PFC, B) midline showed this effect, along with left ventrolateral PFC (C). Bars reflect difference in hippocampal connectivity between subsequently remembered and forgotten. Error bars denote standard error.