Testing Promotes Long-Term Learning via Stabilizing Activation Patterns in a Large Network of Brain Areas

Cerebral Cortex November 2014;24:3025–3035 doi:10.1093/cercor/bht158 Advance Access publication June 24, 2013 Testing Promotes Long-Term Learning via Stabilizing Activation Patterns in a Large Network of Brain Areas Attila Keresztes1, Daniel Kaiser2, Gyula Kovács1,2,3,4 and Mihály Racsmány1 1 Department of Cognitive Science, Budapest University of Technology and Economics, Budapest, Hungary, 2Institute of Psychology, University of Regensburg, Regensburg, Germany, 3DFG Research Unit Person Perception, FriedrichSchiller-University of Jena, Jena, Germany and 4Institute of Psychology, Friedrich-Schiller-University of Jena, Jena, Germany Address correspondence to M. Racsmány, Budapest University of Technology and Economics, Egry József u.1., Budapest, Hungary. Email: Gyula Kovács and Mihály Racsmány contributed equally to this study. Keywords: fMRI, forgetting, long-term learning, retrieval, testing effect Introduction Understanding the neural basis of how we lose access to previously encoded knowledge is a fundamental question of cognitive science as well as the psychology of learning and education. Since the seminal work of Ebbinghaus (1885/ 1964), the effect of the retention interval on forgetting has been one of the central topics of memory research. Several factors have been identified that could potentially explain aspects of the strong connection between retention interval and forgetting. Two such factors are the negative effect of acquiring new information after encoding the target event and the effect of sleep on memory consolidation (Roediger et al. 2010). Although some core processes of forgetting—such as the failure of memory consolidation and the consequences of interference resolution from competing irrelevant memories during retrieval—have already been identified (Uncapher and Wagner 2009; Wimber et al. 2009; Levy et al. 2010), our knowledge of the neural mechanisms of long-term forgetting is far from comprehensive. Hence, it is not surprising that some of the most remarkable experimental results regarding forgetting are those that demonstrated that even a single factor (an additional retrieval after memory encoding) can significantly reduce the negative influence of retention interval on recall © The Author 2013. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: performance (Spitzer 1939; Tulving 1967; Carrier and Pashler 1992; Roediger and Karpicke 2006a). The finding that additional retrieval practice promotes better long-term retention and a slower forgetting rate than the simple restudy of the same information has been termed the “testing effect,” an effect that is currently attracting considerable attention (Roediger and Butler 2011). This phenomenon contradicts what is typically thought about successful learning and is also in conflict with general educational practice, in which testing is only the checkpoint of consecutive study phases (Roediger and Karpicke 2006b). Furthermore, recent experiments have demonstrated that the rate of forgetting is influenced by learning strategy. Although retesting had no mnemonic advantage over restudying at short retention intervals, it produced significantly higher learning performance than an equal amount of restudying when the retention interval was longer than 1 day (Wheeler et al. 2003; Karpicke and Roediger 2008; Toppino and Cohen 2009). These results suggest that the efficiency of testing over restudying has a positive correlation with the length of retention interval. Although this interaction between learning strategy and retention interval seems to be an important aspect of human learning, the responsible functional neural networks have not yet been identified. As a first step in seeking for the neural correlates of the testing effect, we investigated areas of the human brain that are known to be involved in cue-driven episodic retrieval (ER) processes. In previous experiments, ER was typically studied with associative cued recall and recognition tasks (Rugg and Henson 2002). These experiments demonstrated that successful memory retrievals are associated with activations in a large cortical network, including the prefrontal (PFC), posterior parietal (PPL), and medial temporal cortices, and hippocampus (Fletcher and Henson 2001; Rugg 2004; Spaniol et al. 2009; Kim 2011). Importantly, this retrieval-related network has a striking overlap with the network activated by working memory (WM) tasks (Cabeza et al. 2002). This result corresponds to WM theories that assume that WM activation is crucial for enhancing the efficiency of retrieval cues in guiding memory search (Bunting 2006; Unsworth and Engle 2006, 2007). Interestingly, 2 recent neuroimaging studies (Kuhl et al. 2007; Eriksson et al. 2011) demonstrated that when compared with a single retrieval, repeated retrieval practice leads to a reduced activation of a large portion of these regions, including the bilateral ventrolateral PFC, inferior frontal cortices (BA 9/44), the right DLPFC (BA 45/46), the left precuneus (BA 39), and the bilateral superior parietal lobule (BA 7). These results The testing effect refers to the phenomenon that repeated retrieval of memories promotes better long-term retention than repeated study. To investigate the neural correlates of the testing effect, we used event-related functional magnetic resonance imaging methods while participants performed a cued recall task. Prior to the neuroimaging experiment, participants learned Swahili–German word pairs, then half of the word pairs were repeatedly studied, whereas the other half were repeatedly tested. For half of the participants, the neuroimaging experiment was performed immediately after the learning phase; a 1-week retention interval was inserted for the other half of the participants. We found that a large network of areas identified in a separate 2-back functional localizer scan were active during the final recall of the word pair associations. Importantly, the learning strategy (retest or restudy) of the word pairs determined the manner in which the retention interval affected the activations within this network. Recall of previously restudied memories was accompanied by reduced activation within this network at long retention intervals, but no reduction was observed for previously retested memories. We suggest that retrieval promotes learning via stabilizing cue-related activation patterns in a network of areas usually associated with cognitive and attentional control functions. Materials and Methods Participants Twenty-nine healthy participants (2 left handed, 20 females, mean ± SD age: 22.93 ± 2.26 years) were recruited at the University of Regensburg. All participants were native German speakers and gave informed written consent to participate in the study, which was approved by the ethics committee of the University of Regensburg. None of the participants had any history of neurological diseases, and all had normal or corrected-to (...truncated)