Memory-related functional connectivity in visual processing regions varies by prior emotional context

Abstract

Memory retrieval involves the reactivation of processes that were engaged at encoding. Using a Generalized Linear Model to test for effects of valence, our prior study (Bowen & Kensinger, in press) suggests memory for information previously encoded in a negative context reengages sensory processing regions at retrieval to a greater extent than positive. Here, we used partial least squares analyses of the same dataset to determine whether this valence-specific processing was one of the dominant patterns in the retrieval data. Trials previously paired with a face revealed a strong pattern of emotion that did not vary by valence, but for trials previously paired with a scene, an extensive network of regions was active during recollection of trials paired with negative content. These same regions were negatively correlated with recollection of trials paired with positive content. These results confirm that, despite no emotional content present during the time of retrieval, strong patterns of emotional study context are present in the data. Moreover, at least for trials paired with scenes at encoding, valence-specific networks are linked to episodic memory recollection, providing further support for recapitulation of sensory processing during recollection of negative emotional information.

Early Reactivation of Emotion in ERPs to Neutral Retrieval Cues

“…In previous fMRI work, including a study using the same paradigm employed in the present study, our lab has shown that neural recapitulation is greater for negatively valenced stimuli than neutral or positive (Bowen & Kensinger, 2017a, 2017b. Only a few studies have examined how emotional content from encoding affects the ERP response at retrieval (Jaeger et al, 2009;Maratos & Rugg, 2001;Smith, Henson, Dolan, & Rugg, 2004).…”

“…In the current work, we employed a paradigm known to elicit greater recapitulation for negative versus positive contexts in fMRI (Bowen & Kensinger, 2017a, 2017b. Neutral words were paired with an unrelated neutral, positive, or negative picture during memory encoding.…”

“…Successful memory for neutral words (Bowen & Kensinger, 2017a, 2017b and line drawings (Kark & Kensinger, 2015, 2019 is associated with greater recapitulation in regions including those within the ventral visual stream to a greater extent for items previously encoded in a negative compared to a neutral or positive context. This is true even though the emotional content is no longer present at the time of retrieval (for a review see Bowen, Kark, & Kensinger, 2018).…”

Prior Emotional Context Modulates Early Event-Related Potentials to Neutral Retrieval Cues

“…To this end, our prior fMRI work has shown that neutral retrieval cues can reactivate some of the emotion-related properties associated with the prior encoding experience. Successful memory for neutral words (Bowen & Kensinger, 2017a, 2017b and line drawings (Kark & Kensinger, 2015 is associated with greater recapitulation in regions including those within the ventral visual stream to a greater extent for items previously encoded in a negative compared with a neutral or positive context. This is true although the emotional content is no longer present at the time of retrieval (for a review, see Bowen et al, 2018).…”

Imagery retrieval may explain why recall of negative scenes contains more accurate detail

“…A finding with important practical and theoretical implications is that negatively, as compared to positively, valenced pictures and scenes are associated with superior recognition and sense of recollection (Ochsner, 2000), particularly with respect to their central visual details (Christianson & Loftus, 1991; Kensinger, 2009; Kensinger, Garoff-Eaton, & Schacter, 2006). Some reasons for this may be that negatively valenced scenes recruit more sensory processing areas at encoding (Kensinger & Schacter, 2008; Mickley & Kensinger, 2008) and that there is a greater recapitulation of this processing at retrieval (Bowen & Kensinger, 2017). Much less is known about the phenomenological processes operating at retrieval that correspond to or could mediate neural differences in the processing of positive and negative scenes.…”