Effect of emotional valence on retrieval-related recapitulation of encoding activity in the ventral visual stream

Abstract

While prior work has shown greater retrieval-related reactivation in the ventral visual stream for emotional stimuli compared to neutral stimuli, the effects of valence on retrieval-related recapitulation of successful encoding processes (Dm effects) have yet to be investigated. Here, seventeen participants (aged 19-35) studied line drawings of negative, positive, or neutral images followed immediately by the complete photo. After a 20-min delay, participants performed a challenging recognition memory test, distinguishing the studied line drawing outlines from novel ones. First, results replicated earlier work by demonstrating that negative and positive hits elicited greater ventral occipito-temporal cortex (VOTC) activity than neutral hits during both encoding and retrieval. Moreover, the amount of activation in portions of the VOTC correlated with the magnitude of participants' emotional memory enhancement. Second, results revealed significant retrieval-related recapitulation of Dm effects (Hits>Misses) in VOTC (anterior inferior temporal gyri) only for negative stimuli. Third, connectivity between the amygdala and fusiform gyrus during the encoding of negative stimuli increased the likelihood of fusiform activation during successful retrieval. Together, these results suggest that recapitulation in posterior VOTC reflects memory for the affective dimension of the stimuli (Emotional Hits>Neutral Hits) and the magnitude of activation in some of these regions is related to superior emotional memory. Moreover, for negative stimuli, recapitulation in more anterior portions of the VOTC is greater for remembered than forgotten items. The current study offers new evidence for effects of emotion on recapitulation of activity and functional connectivity in support of memory.

Keywords: Amygdala; Emotion; FMRI; Memory; Recapitulation; Ventral visual stream.

Figure 1

Stimuli and task structures. a) During encoding, participants were shown line drawing outlines of IAPS images (1.5 seconds), followed by the complete color photo (2 seconds). Participants made an approach/back away judgment during the presentation of each photo. b) During the recognition task, participants were shown studied line drawings intermixed with novel line drawings. At both encoding and recognition, fixation periods between trials were jittered (0.5–9.5s). c) Sample of line drawings of IAPS images.

Figure 2

Regions showing significant spatial overlap for emotional hits compared to neutral hits and correlations with emotional memory enhancement in VOTC. Compared to neutral items, conjunction analysis confirmed greater encoding-to-retrieval overlap in VOTC for negative hits (in red) and, positive hits (in blue), with some overlap between these regions (in cyan). Emotional memory enhancement at retrieval was positively correlated with VOTC activation (activity in green and yellow). See Table 1 and Supplementary Table 1 for list of all regions.

Figure 3

Retrieval-related recapitulation of Dm effects for negative hits in ITG. Conjunction analysis revealed extensive overlap in VOTC regions recruited during successful encoding and retrieval of negative stimuli (in red, see Table 2 and Supplementary Table 2 for all regions.). Regions of the ITG that showed a significant valence by response type interaction are shown in green (Negative Hits > Misses, Positive Misses > Hits; joint probability p < 0.005), with the spatial overlap of the joint probability maps shown in yellow.

Figure 4

Recapitulation of amygdala connectivity related to Dm effects for negative information. Amygdala seed region for all gPPI analyses visualized on the average of the anatomical scans for the seventeen participants (shown in violet). Conjunction analysis revealed that regions of the left fusiform gyrus that were engaged with the amygdala during successful encoding of negative items were reactivated during retrieval of negative items (shown in red). See Table 3 for all regions.