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-minute 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.

Recapitulation of emotional source context during memory retrieval

“…Items studied in a neutral context showed left lateralized overlap in middle temporal gyrus (BA 21; MNI: −60, −40, −4, k = 31) shown in green in Figure 4. This pattern of results of greater reactivation in sensory cortices for negative valence is consistent with Kark and Kensinger (2015), as detailed in the introduction. The reverse analysis of Misses > Remember Hits did not reveal any overlap that survived thresholding for negative or positive valence, but there was significant recapitulation for Neutral Misses > Neutral Remember Hits.…”

“…The fMRI analyses were used to 1) examine whether valence-based recapitulation occurs generally for hits or whether the recapitulation is enhanced for recollection compared to other processes (i.e., familiarity and forgetting); 2) replicate and extend prior work (Kark & Kensinger, 2015) showing greater reactivation in sensory regions for successful memory of negative stimuli compared to successful memory of positive or neutral stimuli; 3) replicate previous findings (e.g., Fenker et al, 2005) showing reactivation of content-specific regions, namely (FFA and parahippocampal place area [PPA]); 4) determine if recapitulation varies not only as a function of valence (negative, positive, neutral), but whether this interacts with stimulus content (i.e., faces or scenes) and memory within content specific ROIs.…”

“…First, by employing a remember/know paradigm, we could test whether recapitulation was disproportionately related to recollection, as would be suggested by many theories regarding the links between recapitulation and conscious re-experience. Second, we could extend Kark and Kensinger’s (2015) findings in several ways. Although the line drawings used in Kark and Kensinger had less emotion than the full IAPS images, emotional content may have still been conveyed by the line drawings.…”

“…In this study (Kark & Kensinger, 2015), participants encoded black and white degraded line-drawing versions of International Affective Picture System (IAPS; Lang, Bradley, & Cuthburt, 2008) images, which were followed by the full colored photograph. After a short delay (20 minutes), participants were given the line-drawings as retrieval cues and asked to make an old or new judgment.…”

Residual effects of emotion are reflected in enhanced visual activity after sleep

“…It is possible that this intermixing encouraged participants to retrieve (explicitly or implicitly) the associated foreground content of the scenes, and that this would not have occurred with a different design. For instance, as emotion has been shown to lead to enhanced sensory processing (e.g., Kark & Kensinger, 2015;Keightley et al, 2011), the presentation of negative objects intermixed with neutral objects and neutral backgrounds during retrieval may have primed visual areas to be globally more active during retrieval (i.e., even during the retrieval of neutral stimuli) relative to a design in which no emotional content was presented. However, this design feature in itself is unlikely to explain differences between the sleep and wake groups, as the recognition lists were identical in those two conditions.…”