Stress and the corresponding release of glucocorticoids modulate declarative human memory (reviews: Het et al., 2005, Joels et al., 2006, Sandi and Pinelo-Nava, 2007 and Shors, 2006). For example, exposure to ice-water (CPT; Cold Pressor Test) directly after presentation of pictures improved memory of the pictures when tested 1 week later (Cahill, Gorski, & Le, 2003). Pharmacologically induced elevations of cortisol levels deteriorated word learning (Kirschbaum, Wolf, May, Wippich, & Hellhammer, 1996). The influence of stress on learning and memory is heterogeneous and varies depending on the emotional content and the valence of stimuli (Buchanan and Lovallo, 2001, Cahill and Alkire, 2003, Cahill et al., 2003, Rimmele et al., 2003, Schwabe et al., 2008 and Southwick et al., 2002), timing of stress (before the learning: Lupien et al., 2002, Maheu, Collicut, et al., 2005 and Schwabe et al., 2008; after the learning: Andreano and Cahill, 2006 and Cahill et al., 2003), the intensity of stress (Andreano and Cahill, 2006, Maheu, Collicut, et al., 2005 and Kirschbaum et al., 1996) and memory type (Kirschbaum et al., 1996 and Luethi et al., 2009). Most studies addressing the influence of stress on memory used paradigms tapping into declarative memory.
In contrast, only a few studies investigated how stress modulates non-declarative memory formation (Kirschbaum et al., 1996, Luethi et al., 2009 and Lupien et al., 1997). In one of these studies, participants were first exposed to a stressor and then performed a battery of memory tasks including classical conditioning with emotionally positive and negative stimuli, as well as perceptual and conceptual priming tasks (Luethi et al., 2009). Stress had no influence on the priming tasks and the only significant effect in the conditioning task was found with negative stimuli. These results indicate that stress may influence non-declarative learning to some extent, however, it is not clear which phase of learning was affected because memory recall was tested shortly after performing the tasks. Hence, little time was allowed for memory consolidation and for the stress response to decline prior to memory recall. For declarative learning, different phases of learning are influenced differently by stress (Het et al., 2005 and Roozendaal, 2002). It is therefore important to systematically study the influence of stress on different phases of learning also for non-declarative learning. Furthermore, previously tested non-declarative learning tasks are rather short-term and may not depend on the post-learning phase, i.e. consolidation, which has been shown to be sensitive to the influence of stress and changes in cortisol levels (Roozendaal, 2002, Sandi, 1998 and Shors, 2006). Here, we used a visual perceptual learning paradigm, known to be sensitive to post-learning manipulations (consolidation), to study how stress influences consolidation of non-declarative perceptual learning.1
Perceptual learning is the ability to learn to perceive (review: Fahle & Poggio, 2002). Visual perceptual learning is a non-declarative form of learning that improves discrimination of basic visual stimulus features including vernier acuity (Crist et al., 1997 and Herzog and Fahle, 1997), contrast (Kuai et al., 2005 and Yu et al., 2004), motion (Ball and Sekuler, 1982 and Liu and Vaina, 1998) and textures (Censor et al., 2006, Karni and Sagi, 1993, Mednick et al., 2005 and Stickgold, LaTanya, et al., 2000). In a texture discrimination task (TDT), participants determine the orientation of an array of target elements within distracter elements (Fig. 1A). Task difficulty is controlled by the ISI (Inter-Stimulus Interval) between the target display and a mask display (Fig. 1A). The ISI limits the temporal availability of a stimulus and reflects the time needed to obtain a workable percept. Thus, the ISI is a measure of perceptual performance and becomes potent with experience (Karni and Sagi, 1991, Karni and Sagi, 1993 and Karni et al., 1994). A short ISI indicates good performance. Importantly, consolidation and sleep are often needed to improve texture discrimination (Censor et al., 2006, Karni et al., 1994, Mednick et al., 2003, Stickgold, Whidbee, et al., 2000 and Yotsumoto, Chang, et al., 2009). For example, performance between two sessions did not improve unless they were separated by a night (Karni and Sagi, 1993, Karni et al., 1994, Stickgold, LaTanya, et al., 2000, Stickgold, Whidbee, et al., 2000 and Yotsumoto, Chang, et al., 2009). Furthermore, training another task directly after the TDT abolished performance improvements (Yotsumoto, Chang, et al., 2009) suggesting that this task is sensitive to post-learning manipulations (see also Beer, Vartak, & Greenlee, 2012). Finally, sleep deprivation increased cortisol levels (Meerlo, Sgoifo, & Suchecki, 2008) and disrupted consolidation of the TDT (Stickgold, LaTanya, et al., 2000). Accordingly, these results suggest that (1) TDT can be disrupted by post-learning manipulations and (2) these manipulations may involve stress and increased cortisol levels.
