The term emotional enhancement in item memory is applied to instances where emotional items in a scene are recalled more frequently than are neutral items. Similarly, the term decrement in memory for backgrounds indicates that backgrounds from scenes containing emotional items are remembered less often than backgrounds from scenes containing neutral items. When both of these conditions (i.e., both enhancement in item memory and decrement in memory for backgrounds) arise within memory for scenes of a particular emotional type, a tradeoff effect has occurred. The magnitude of the trade-off in memory observed for emotional scenes is in relation to one’s memory ability for neutral scenes, respective of one’s overall memory ability. In this way, calculation of the trade-off effect takes into account individual variations between those persons with overall ‘good’ or ‘poor’ memory ability, and the magnitude of the trade-off observed is not driven by the circumstance of some persons having an overall more limited memory capacity, which would be present across all types of scenes.
We first established the presence of a trade-off effect in the behavioral results. Then an interaction contrast on the neuroimaging data identified the pattern of activation corresponding with an emotional enhancement in item memory and decrement in memory for backgrounds, thereby revealing the regions predicting a trade-off in memory for emotional scenes. Closer examination of the activation in regions identified within this contrast allowed further illustration of the effects of emotion upon the memory trade-off. Neuroimaging techniques additionally permit isolation of the encoding-related neural activity that specifically predicts selective memory for an emotional item without its background in emotional scenes, compared to the activity predicting good memory for both components from emotional scenes. These analyses identify regions exclusively associated with selective item memory as distinct from regions more broadly responding to the emotional item within the scene, irrespective of memory for the background.
Although the background components from scenes were all neutral in valence and not inherently arousing, the type of emotion assigned to backgrounds within analyses are defined by the identity of the item with which they had been paired in a scene during a prior study session (e.g., “high arousal background” indicates a background, such as a river, that had been studied as part of a scene containing a high arousal item, such as a snake).
3.1 Behavioral data
Behavioral responses were analyzed using corrected recognition scores of hits minus false alarms (reported in ). Corrected recognition rates were calculated to consider differences in participants’ biases to say “old” to test items. There was no significant interaction between the magnitude of the trade-off and gender (F
s(1,17)<1.00), so data from men and women were combined in all analyses2
Corrected recognition and false alarm rates
To establish to presence of a trade-off in behavioral memory performance, we conducted an ANOVA with factors of component (items, backgrounds) and scene type (lower arousal positive, higher arousal positive, lower arousal negative, higher arousal negative, neutral) on the corrected recognition scores. This ANOVA produced significant main effects of component (F
<.0005, partial η2
=.86) and emotional scene type (F
<.003, partial η2
=.63) qualified by an interaction between component and scene type (F
<.0005, partial η2
=.83). The interaction between component and scene type reflects a trade-off effect, with an enhancement in memory for emotional items and a decrement in memory for backgrounds presented within emotional scenes relative to neutral scenes (), replicating the pattern of behavioral results reported in Waring & Kensinger (2009)
. Additionally, we computed T-tests contrasting memory for emotional scene components each compared to neutral (e.g., positive lower arousal items compared to neutral items, negative low arousal backgrounds compared to neutral backgrounds). There was a significant enhancement in memory for four types of emotional items compared to neutral (all t
<.005). There was a significant decrement in memory for backgrounds from emotional scenes compared to neutral scenes (all t
<.03) except for positive higher arousal scenes for which the numerical difference did not reach significance (t
=.25). Taken together these results show that the enhancement in memory for emotional items is present in all scene types, but the trade-off in memory is less likely to arise in scenes containing positive higher arousal items.
Magnitude of the trade-off in memory by scene valence and arousal characteristics
We analyzed the pattern of response times for the study phase approach/retreat decision between emotional scenes to find whether the effect of scene valence or arousal on the magnitude of the trade-off could be explained by the amount of time taken to consider the approach/retreat decision during the study phase. These response times reflect the amount of time to make the decision but not the total amount of time spent viewing the scene; participants viewed all scenes for a uniform time period (3 sec.), regardless of speed of responding. An ANOVA of response times with factors of scene type (lower arousal positive, higher arousal positive, lower arousal negative, higher arousal negative, neutral), component (item, background) and memory (remembered, forgotten) showed a main effect of scene type (F(4,15)=18.62, p<.0005, partial η2=.83), reflecting that response times were fastest for higher arousal negative scenes (m= 1.44 sec), slower for lower and higher arousal positive scenes and neutral scenes (all m = 1.59 sec), and slowest for lower arousal negative scenes (m=1.65 sec). The ANOVA also revealed an interaction between the factors of component and memory (F(1,18)=6.17, p<.03, partial η2=.26), where response times for items were unaffected by whether the item was subsequently remembered or forgotten (remembered items m = 1.56 sec, forgotten items m = 1.58 sec), but response times to scenes for which the background was subsequently forgotten were faster than to those scenes for which the background was subsequently remembered (forgotten backgrounds m = 1.54 sec, remembered backgrounds m = 1.61 sec). Importantly, there were no significant 2- or 3-way interactions between scene type and component or memory in the pattern of response times data (all p>.05), indicating that the response times did not affect memory for scene components significantly differently between the types of scenes. These results suggest that response time differences could contribute to the occurrence of selective item memory in general, but that across scene types, variability in response times for the encoding task cannot explain why there would be differences in the tradeoff effect between different types of emotional scenes.
3.2 Neuroimaging data
Having demonstrated a trade-off in memory for all four types of emotional scenes, we wanted to examine the neural processes that led to those effects. We conducted an interaction contrast on the neuroimaging data to identify the regions predicting a trade-off in memory for emotional scenes, revealing the pattern of activation corresponding with an emotional enhancement in item memory and a decrement in memory for backgrounds. This contrast for correctly recognized scene components was defined as: (emotional – neutral when only the item remembered) – (“emotional” – neutral when only the background remembered); i.e., ([(lower arousal positive item only + higher arousal positive item only + lower arousal negative item only + higher arousal negative item only) – (neutral item only)] – [(lower arousal positive background only + higher arousal positive background only + lower arousal negative background only + higher arousal negative background only) - (neutral background only)]). Results of this interaction contrast showed that there is activation common to the trade-off among the four types of emotional scenes within a network of regions frequently associated with successful emotional memory (Adolphs et al., 2001
; Dolcos et al., 2004
; Kensinger & Schacter, 2008
; Mather et al., 2006
). These regions included the inferior and medial frontal gyrus, anterior cingulate cortex (ACC), left and right amygdala, thalamus, hippocampus, superior temporal gyrus, fusiform gyrus, and a large area along the middle temporal gyrus that was particularly left lateralized (see ).
Regions corresponding with the trade-off in memory for emotional scenes (i.e., showing an enhancement in memory for emotional items but not backgrounds).
We performed additional analyses within six regions-of-interest identified from the interaction contrast that are part of the traditional emotional memory network, in order to better understand the effects of emotion upon the memory trade-off within these regions. Regions of the inferior frontal gyrus (−46, 16, 14), right amygdala (26, 1, −12), left amygdala (−26, −5, −13), fusiform (−42, −42, −15), hippocampus (−32, −29, −4), and temporal pole (34, 1, −12) were selected for these further analyses (all coordinates refer to Talairach coordinates). We computed ANOVAs for each ROI to assess effects of 4 emotional scene types (lower arousal positive, higher arousal positive, lower arousal negative, higher arousal negative) upon the encoding–related activation that was associated with remembering an emotional item while forgetting its paired background in the scene. There were no significant effects of scene emotional content upon the encoding-related activation that was associated with remembering an emotional item while forgetting its paired background in the scene (Fs(3,15)<2.2, p>.13, partial η2< .31). These results indicate that a core set of regions is associated with the trade-off for emotional scenes, and that these regions are not involved differently based upon specific scene arousal or valence characteristics.
The interaction contrast reported above was chosen to mirror the way in which the tradeoff is behaviorally defined: as a comparison between the successful memory for elements of emotional compared to neutral scenes. Yet part of the reason why trade-offs are typically defined in relation to neutral scenes is because there is no behavioral measure of what happens when an item is remembered and a background is forgotten within a single scene; the proportion of time that this occurs is only meaningful in relation to a neutral scene baseline. By contrast, neuroimaging techniques permit the comparison of the neural signatures predicting successful item memory when the background of the scene is later remembered versus later forgotten. Therefore, contrasting the neural activity during encoding that predicts selective memory for the emotional item without its background compared to the activity predicting good memory for both components from emotional scenes (i.e., item only > item + background) can be additionally informative. In other words, is there a set of regions exclusively associated with the trade-off effect, or does this pattern of activation more generally reflect the response to the emotional item within the scene, irrespective of whether the background from the scene was remembered or forgotten? To answer this question we contrasted activation associated with remembering only the emotional item while forgetting the background versus remembering the emotional item and background that is common among all four emotional scene types ([lower arousal positive item only + higher arousal positive item only + lower arousal negative item only + higher arousal negative item only] > [lower arousal positive item and background + higher arousal positive item and background + lower arousal negative item and background + higher arousal negative item and background]). This contrast revealed that activation uniquely associated with selective item memory is found mainly within temporo-parietal regions, such as the inferior parietal lobule and middle temporal gyrus (see ). The regions identified here indicate the areas that are necessary for selective attention upon an emotional item in the scene, to the detriment of memory for the background of the scene. These regions are not all present in the interaction contrast because this contrast did not specify the regions exclusively associated with selective attention for items within emotional scenes; the same regions revealed here may be necessary for allocation of attentional resources toward items within neutral scenes. The regions identified in this contrast, but not in the interaction contrast previously described, are the areas necessary for attention to emotional items when the background is later forgotten versus later remembered, however they are not exclusive of those regions that may also be active for attention to neutral items.
Regions corresponding with the trade-off in memory for all emotional scenes. (trade-off > item and background remembered)
Further, we examined whether there are certain regions associated with selective memory for emotional items depending upon the specific valence and arousal characteristics of the item within the scene, beyond those regions commonly activated among all 4 types of emotional scenes. We examined how the set of regions associated with selective item memory in each of the four types of emotional scenes is distinct from the other three types (e.g. positive lower arousal item only > [positive higher arousal item only + negative lower arousal item only + negative higher arousal item only]). These analyses identified the set of regions supporting selective memory for items from each of the four emotional scene types.
These four contrasts indicated that in addition to the core network of regions associated with the trade-off among all types of emotional scenes, there are additional networks of regions active for selective item memory in each of the four types of emotional scenes. The pattern of activation supporting selective memory for positive lower arousal items showed a small set of regions including portions of the medial and middle frontal gyri, anterior cingulate, and middle occipital gyrus (see ). The selective memory for positive higher arousal items was associated with a larger set of regions widely distributed across the prefrontal cortex (BA 6, 8, 9 10, 11, 46, 47), as well as cingulate gyrus and bilateral regions of the fusiform (see ). The selective memory for negative lower arousal items was predicted by activation mainly with middle occipital gyrus, cuneus, and middle frontal gyrus (see ). Lastly, the negative higher arousal item selective memory corresponded with activation in the left fusiform (see ). As depicted in , these regions were largely unique and non-overlapping, with small areas of common activation among positive and negative lower arousal scenes in the left middle frontal gyrus and left cuneus/middle occipital gyrus, and among positive and negative higher arousal scenes within the left fusiform.
Regions corresponding with the trade-off in memory for positive low arousal scenes. (trade-off > item and background remembered)
Regions corresponding with the trade-off in memory for positive high arousal scenes. (trade-off > item and background remembered)
Regions corresponding with the trade-off in memory for negative low arousal scenes. (trade-off > item and background remembered)
Region corresponding with the trade-off in memory for negative high arousal scenes. (trade-off > item and background remembered)
Activation predicting a trade-off in memory between emotional scene types