Elsevier

NeuroImage

Volume 26, Issue 3, 1 July 2005, Pages 829-838
NeuroImage

Emotional context during encoding of neutral items modulates brain activation not only during encoding but also during recognition

https://doi.org/10.1016/j.neuroimage.2005.02.045Get rights and content

Abstract

In general, encoding of neutral material includes the context in which the respective material is learned. The effect of emotional context on successfully encoded neutral material has been investigated only recently in few studies, but the main underlying mechanisms are still fairly unknown. In the present study, we investigated the effect of positive and negative emotional context on encoding and later recognition of neutral items. We could demonstrate that brain activation not only during encoding but also during recognition of neutral items depended on the emotional valence of the encoding context. Whereas activation of medial temporal lobe structures during encoding specifically predicted subsequent memory when learning appears in a positive emotional context, activation of the anterior temporal cortex in a region with afferent input to the amygdala predicted memory for material learned in negative context. Recognition of items encoded in positive emotional context revealed activation of hippocampal and medial prefrontal regions, recognition of items encoded in negative emotional context revealed activation of the caudate nucleus. We assume that our findings reflect the recruitment of different brain circuits depending on the emotional context during learning.

Introduction

Greater brain activation during encoding for later successfully remembered compared to forgotten material, a so-called subsequent memory effect (SME), has been demonstrated in a number of studies in humans by means of functional neuroimaging techniques and intracerebral recordings (Paller and Wagner, 2002). It has been shown that activation in regions of the prefrontal cortex and the medial temporal lobe can predict subsequent memory (Brewer et al., 1998, Erk et al., 2003, Fernandez et al., 1999, Fletcher et al., 2003, Otten et al., 2001, Wagner et al., 1998). The SME has been investigated mainly for neutral items, e.g., words. However, considerable evidence shows that memory for emotional material is enhanced, particularly for negative material (Adolphs et al., 1997, Cahill et al., 1994, Cahill et al., 1996). Meanwhile, an SME has also been investigated for emotional material (Dolcos et al., 2004). Successful encoding activity in the amygdala and medial temporal lobe memory regions was greater for emotional events and activation of both regions was strongly correlated. Moreover, it has been shown that activity in the anterior hippocampus predicts memory for emotional items, whereas activity in the posterior hippocampus predicts memory for neutral items. However, this study investigated memory for the emotional content. Thus, the effects of the emotional state and effects of the material itself cannot be distinguished. An important question is, whether the emotional context during encoding influences subsequent memory and if so, of what kind, behaviorally and neurally, this influence is. Up to now, only a few functional imaging studies exist, which investigated the effects of emotional context on subsequent memory. In two studies, one using event-related potentials (ERP) and one using fMRI, subjects had to recognize neutral words previously learned in the context of positive, negative, or neutral sentences. In the ERP study, retrieval of words encoded in negative sentences reveals left parietal and right frontal potentials (Maratos and Rugg, 2001). In the fMRI experiment, retrieval of words encoded in negative relative to neutral sentences shows activation of dorsolateral prefrontal and medial temporal, i.e., amygdala and hippocampal activation (Maratos et al., 2001). Two other studies using ERP and fMRI, respectively, tested the effect of emotional context by forming associations between a neutral visual object with an emotional background stimulus. ERPs show lateral temporal and left temporo-frontal potentials for retrieval of objects associated with emotional backgrounds (Smith et al., 2004a). The respective fMRI study reported prefrontal, hippocampal, and parahippocampal activation for the retrieval of objects previously associated with emotional relative to neutral backgrounds (Smith et al., 2004b). In a study of our own group, we investigated the modulatory effect of emotional context on brain activation during successful encoding. We could demonstrate that, during positive context, recall was predicted by activation in parahippocampal and extrastriate brain areas, whereas during negative encoding context, recall was predicted by amygdala activation (Erk et al., 2003). In our previous experiment, we used a free recall procedure instead of a recognition task because the influence of emotional context has been found in behavioral studies particularly in tasks requiring active recovering of information from memory, which is more likely in recall than in recognition (Doerksen and Shimamura, 2001, Fiedler, 1991).

Based on these findings, the aims of the present study are (1) to test the influence of the retrieval mode for the SME at the behavioral and especially at the neural level and (2) to test the impact of the emotional context during encoding of neutral material on successful recognition processes, when the retrieval procedure has no emotional context information (i.e., is “neutral”). Behavioral evidence shows that the effect of emotion on memory is generally stronger for active retrieval tasks like free recall, and that free recall is supported by positive mood, which–in contrast to negative mood–triggers creative problem solving which in turn is useful for free recall (Ashby et al., 1999, Fiedler, 2001). In contrast, negative mood subserves tasks which afford maximum avoidance of mistakes and thus subserves more passive tasks like recognition. Avoidance behavior has to be perfectly reliable, and attentive to potentially threatening stimuli. Thus, whereas negative mood supports conservative functions like sticking to the stimulus facts and avoiding mistakes, positive mood supports the more creative function of active generation of information, and inferences based on prior knowledge. Mood effects are strongest when active processes take place which transform the input (Fiedler, 1991). Thus, we expected (1) that by using a passive retrieval mode, i.e., a recognition task, we will not find a behavioral effect of encoding context for memory performance and if any effect occurs, it should be an advantage effect of negative context. Furthermore, we assume that, during successful encoding in positive and negative emotional contexts, different information processing procedures are subserved by different neural circuits. We expected medial temporal regions being crucially involved in encoding, with the parahippocampal gyrus in learning during positive context and the amygdala in learning during negative context.

Using a passive recognition task provides the opportunity to easily test the neural effects of retrieval processes. We predicted (2) that during the recognition procedure, similar brain regions were recruited as for the encoding procedure, depending on the context during learning. This prediction is based on a recent proposal that, during encoding, associations are incidentally formed, e.g., by providing the originally neutral material with an emotional “tag” (Lewis and Critchley, 2003), and that this information is retrieved during recognition of the original item.

Section snippets

Subjects

Ten right-handed subjects [three female, mean age 24.3 (range 21–27) years] without any history of medical or neurological illness participated in the study. All subjects gave written informed consent. The study was approved by the local ethics committee.

Data acquisition

FMRI data were acquired on a 1.5-T Siemens Magnetom Symphony whole-body MRI-system equipped with a head coil. T2*-weighted functional images were obtained using echo planar imaging in axial orientation. Image size was 64 × 64 pixel with an FoV

Behavioral results

As expected, recognition rate was much higher when using a passive retrieval task than using an active free recall procedure. Whereas the ratio of retrieved and forgotten items during active retrieval in our previous study was about 25 to 75%, in the present study using a passive recognition procedure, this ratio was reversed. Recognition rate for neutral words did not differ between positive (79.6%) and negative (78.8%) encoding trials. No significant differences were found for reaction times

Discussion

Following previous research (Erk et al., 2003), the present study was set up to investigate the modulatory effects of emotional context on subsequent memory during encoding and recognition. At the behavioral level, emotional context did not influence subsequent memory performance. This corresponds to our primary hypotheses that by using a passive retrieval mode, i.e., a recognition task, we will not find an effect of encoding context for memory performance. This is in line with other studies

Conclusion

In the present study, we manipulated the emotional context during encoding of neutral items. We were interested in the modulatory effect of the emotional context on encoding by investigating the subsequent memory effect. Moreover, we were interested in the effect the encoding context has on recognition, by testing the successful recognition effect. Assuming that an implicit association between item and context will take place, e.g., by a “tagging” of the neutral item, we hypothesized different

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