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Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search

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Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search Thomas Geyer1*., Hermann J. Mueller1,2., Leonardo Assumpcao2, Steffen Gais1 1 Department Psychologie, Ludwig-Maximilians-Universita¨t, Mu¨nchen, Germany, 2 Department of Psychological Sciences, Birkbeck College, University of London, London, United Kingdom Abstract In repeated visual search tasks, facilitation of reaction times (RTs) due to repetition of the spatial arrangement of items occurs independently of RT facilitation due to improvements in general task performance. Whereas the latter represents typical procedural learning, the former is a kind of implicit memory that depends on the medial temporal lobe (MTL) memory system and is impaired in patients with amnesia. A third type of memory that develops during visual search is the observers’ explicit knowledge of repeated displays. Here, we used a visual search task to investigate whether procedural memory, implicit contextual cueing, and explicit knowledge of repeated configurations, which all arise independently from the same set of stimuli, are influenced by sleep. Observers participated in two experimental sessions, separated by either a nap or a controlled rest period. In each of the two sessions, they performed a visual search task in combination with an explicit recognition task. We found that (1) across sessions, MTL-independent procedural learning was more pronounced for the nap than rest group. This confirms earlier findings, albeit from different motor and perceptual tasks, showing that procedural memory can benefit from sleep. (2) Likewise, the sleep group compared with the rest group showed enhanced context-dependent configural learning in the second session. This is a novel finding, indicating that the MTL-dependent, implicit memory underlying contextual cueing is also sleep-dependent. (3) By contrast, sleep and wake groups displayed equivalent improvements in explicit recognition memory in the second session. Overall, the current study shows that sleep affects MTL-dependent as well as MTL-independent memory, but it affects different, albeit simultaneously acquired, forms of MTL-dependent memory differentially. Citation: Geyer T, Mueller HJ, Assumpcao L, Gais S (2013) Sleep-Effects on Implicit and Explicit Memory in Repeated Visual Search. PLoS ONE 8(8): e69953. doi:10.1371/journal.pone.0069953 Editor: Michael J. Proulx, University of Bath, United Kingdom Received January 18, 2013; Accepted June 14, 2013; Published August 2, 2013 Copyright: ß 2013 Geyer et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported by Deutsche Forschungsgemeinschaft (DFG, www.dfg.de) Research Grants GE 1889/1-1 (TG), GA 730/3-1 (SG), and CoTeSys (Cognition for Technical Systems) Excellence Cluster 142 (HM). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] . These authors contributed equally to this work. Introduction contextual cueing has been shown to occur only for a limited number of repeated displays [5–8]. Furthermore, when asked to An important feature of the human brain is its ability to adapt to explicitly recognize previously presented target-distractor config- repeated stimulation by extracting recurring information and urations, observers are able to reliably tell apart at least some of modifying behavior accordingly. Nearly all brain systems con- the repeated from non-repeated displays [5,8]. Importantly, Geyer cerned with perception, cognition, and action control have this et al. [5] also showed that contextual cueing can manifest for a adaptive ability in one way or another. Previous research has given display independently of whether or not this item is explicitly identified different memory systems, which are distinguishable recognized. This suggests that context-dependent configural according to how and what information is stored about previous learning and explicit knowledge of repeated configurations are experiences. Typically, different types of tasks are used to supported by separate memory processes. investigate different forms of memory. However, there are Other investigations of contextual cueing have shown that the paradigms that permit multiple forms of memory to be examined effect is highly flexible. Target-distractor contingencies acquired simultaneously. One of these paradigms is ‘contextual cueing’. with a particular set of stimulus attributes can transfer to other Contextual cueing refers to the phenomenon that visual search is stimulus attributes. Such transfer effects have been reported for facilitated by repeated presentation of target-distractor configura- stimulus features, dimensions, modalities, and the specific search tions, compared with novel, non-repeated arrangements. That is, task performed by observers [3,9–11]. These findings suggest that search reaction times (RTs) are usually faster for repeated relative contextual cueing is independent of the search items’ perceptual to non-repeated displays – an effect which emerges after some attributes, but rather supported by a spatial long-term memory 100–150 trials on the task and can persist for several days [1,2]. that stores associations between the target and the distractor This benefit is usually attributed to implicit perceptual memory for arrangement, or between individual target-distractor pairs [12,13]. spatial (configural) target-distractor contexts, guiding focal atten- Regarding the brain mechanisms underlying contextual cueing, it tion more rapidly to the target location [3,4]. Interestingly, has been demonstrated that the medial temporal lobe (MTL) PLOS ONE | www.plosone.org 1 August 2013 | Volume 8 | Issue 8 | e69953 Sleep-Effects in Repeated Visual Search supports learning of repeated configurations in visual search (for a College, Queen Mary’s College, and University College London review, see [14]). A number of recent fMRI studies provide (University of London), who volunteered their services within an evidence that the perirhinal and entorhinal cortices in particular informal inter-collegiate participants exchange scheme. The are contributing to contextual cueing [15,16]. Moreover, patients remaining 11 observers were recruited from various backgrounds with lesions to the MTL also show impaired contextual cueing outside the academic environment and paid at a rate of Euro 10 [17,18]. Importantly, the neural substrates of contextual cueing per hour. Observers were recruited via university advertisement are different from those mediating other aspects of visual search, and social networks. All observers had normal or corrected-to- such as attention or gaze control, with the latter being supported normal vision and had no history of neurological, psychological, or by neocortical (e.g., frontal and parietal eye fields) and subcortical any other chronic illnesses. All observers gave written informed (e.g., superior colliculus and thalamus) brain structures (for a consent prior to their participation. Participants were instructed to review, see [19]). have between 7 and 8 hours of sleep the two nights preceding the Given the bulk of evidence pertaining to the issue of sleep- experiment. Further, they were told not to drink caffeine or dependent consolidation in the domains of declarative (e.g. [20]) alcohol 24 hours prior to and during the experimental day. Before and procedural memory (e.g. [21]), recent studies have examined the experiment, they filled in a short questionnaire assessing the whether different forms of memory within these domains are quality of their nocturnal sleep preceding the experimental day. differentially affected by sleep. For instance, it has been suggested They entered their ratings on a 5-point scale, ranging from 5 (very that recall is more strongly influenced by sleep than recognition good) to 1 (very bad). Overall, the ratings did not differ between [22], and that awareness modifies the degree to which procedural the two experimental groups: nap, M = 3.46, SD = 0.96, versus memory benefits from sleep [23]. Contextual cueing lends itself rest: M = 3.76, SD = 1.01. particularly well to the investigation of such differential aspects of The experiment consisted of a training and a test session, both memory for several reasons. First, using this paradigm, procedural conducted in a quiet and dimly lit laboratory cubicle at Birkbeck learning can be studied by examining practice-dependent gains in College, Department of Psychological Sciences. During both mean RTs both within and across experimental sessions. Second, sessions, participants performed a contextual cueing task. The first implicit, MTL-dependent contextual cueing can be investigated by session took place in the morning between 9 am and 10 am and comparing RT performance between repeated and non-repeated lasted about 50 minutes; the second session in the evening between search displays. Faster RTs are expected for repeated displays, 5 pm and 6 pm, lasting 15 minutes. After the first session, because display repetition promotes the acquisition of an implicit participants were randomly assigned to a nap (N = 13) or rest spatial-associative memory for the item configuration. Third, group (N = 13). The use of a between-subject
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