Remembering faces: The effects of emotional valence and temporal recency

Highlights

• ERPs were recorded during recall of faces varying in valence, sex, learning context and temporal recency.

• Anterior N2 and FN400 were sensitive to face familiarity (with no difference between overlearned and recent faces).

• Parietal late positivity was sensitive to engram temporal recency and face sex.

• Emotional content can overcome temporal recency thus improving memory recall of recent learnt items.

Abstract

It is known that the longer an information has been memorized, the stronger is its memory trace, and that emotionally-valenced information is more solid than neutral one. We investigated whether the emotional content of recent information might enhance its memory, making it as familiar as information known for a long time. We compared ERPs alternately recorded in response to old and solid information from long term memory (i.e., faces of popular movie stars), to recently acquired emotional information (faces of fictional characters), and to completely new information (faces of previously unknown people). Initially participants familiarized with the fictional police dossiers of 10 victims of dramatic deaths (recent faces), twice a day for seven days before EEG recordings. Recent faces were compared with faces of movie stars and unknown faces in an old/new recognition task. N200 and FN400 responses were affected by face familiarity (with no difference between old and recent faces), while parietal late positivity (LP) was sensitive to temporal recency, being it greater to old than recent faces. Interestingly, LP amplitude was similar for old and recent own-sex faces (victims) that were therefore equally memorable. It is shown that emotional memory can overcome temporal recency thus improving memory recall.

Introduction

The goal of present study was to investigate whether the emotional content of an information might act as a memory enhancer, able to strengthen and consolidate recent, therefore weaker, traces in virtue of their emotional valence.

At this aim we designed an old/new memory paradigm in which faces of popular movie stars known for at least 5–8 consecutive years (therefor “old” faces), were contrasted with recently learned faces of fictional characters studied during the week preceding the EEG recording (“recent” faces) as opposed to previously unknown faces (“new” faces). The time course and functional properties of ERP responses elicited during face recognition were compared. In this way the effect of temporal recency on face remembering was investigated, by considering the gradient: old, recent, and new. Previous literature (e.g., Moreton & Ward, 2010) investigated the extent to which retrieval from long-term memory differs as a function of the retention time. In Moreton and Ward (2010), for example, participants were given 4 min to recall autobiographical events from the last 5 weeks, the last 5 months, or the last 5 years, and the results showed similar retrieval rates. This results has been interpreted in the light of the so-called SIMPLE model (Brown, Neath, & Chater, 2007), according to which correct memory recognitions would be a function of the relative temporal distinctiveness of the items to be remembered, not just of their recency. However, the neuroscientific literature provides evidence of a different neural representation of short vs. long term memories. For example, it has long been known that in case of damage to hippocampal or medial temporal regions, the retrograde amnesia deficit involves only the recent past (for example memories relative to the last few years preceding the cerebral insult) and not the remote past of the patient, thus indicating a greater strength of older memory traces (“Consolidation theory” by Manns, Hopkins, & Squire, 2003, see also Markowitsch and Staniloiu, 2013, Kopelman and Bright, 2012). In addition, according to the “Episodic-to-semantic shift” theory, also called “semanticisation”, episodic memories would acquire a more ‘semantic’ form as they get older, thereby protecting them against the effects of brain damage (Cermak, 1984) or oblivion. Furthermore neurophysiological data have provided multiple evidences that brain encoding of very recent memories would have a bioelectrical nature (e.g. Zamora, Corina, & Ojemann, 2016), while the deep encoding in LTM would be based on plastic structural changes and dendritic formations, also called long-term potentiation (LTP). Interestingly, evidences have been provided that working memory might also involve activity-silent neural states, especially at prefrontal level (Stokes, 2015).

Notwithstanding that, not many studies in humans have directly compared the neural markers of remembering information of different temporal recency, especially with the ERP technique, which is actually very sensitive to both recollection and familiarity processes. Stimuli recognized as known (as opposed to unknown) typically modulate the amplitude of two ERP components: a mid-frontal negativity FN400 sensitive to stimulus familiarity (Curran, 1999, Curran, 2000) and parietal old/new late positivity, indexing stimulus conscious recollection (Evans and Wilding, 2012, Hoppstädter et al., 2015, Rugg et al., 1996, Wilding and Rugg, 1996, Wilding and Sharpe, 2003). According to the dual-process model of recognition memory, judgments produced on the basis of familiarity are quick, automatic, and reflect a general feeling of knowing that a stimulus was previously presented. On the other hand, recollection requires actively reporting details about studied items and results in slow, more effortful judgments (Aggleton and Brown, 1999, Atkinson and Juola, 1974, Yonelinas et al., 1999, Yonelinas et al., 2002).

The present research applied the ERP technique to investigate whether emotional valence might affect recollection of recent memories with respect to old memories. We sought to comprehend if the possible memory enhancement involved face familiarity (N2 and FN400) and/or recognition (LP) and source memory (indexed by frontal responses, such as Late anterior negativity, LAN). In fact, a frontally distributed N400 (FN400), has been directly related to the concept of familiarity. For example, Curran (Curran, 1999, Curran, 2000) found an enhanced negative response between 300 and 500 ms post-stimulus at scalp anterior regions, which was larger to new than old items. Additionally, we expected a modulation of an earlier familiarity-related response (frontal N2) recently found to precede F/N400 effects, and being also larger to unknown than familiar items (Lawson et al., 2012). On the other hand, as previously mentioned, the parietal old/new LP has been associated to stimulus conscious recollection (Wilding and Rugg, 1996, Wilding and Sharpe, 2003).

At this aim the temporal course of brain bioelectrical activity was measured during recognition of faces of different emotional valence, sex, learning context and temporal recency. The study involved the presentation of 300 faces: some belonged to famous people (movie and TV stars), others were learned during a study phase starting one week before the experiment (very recent material), and the remaining were new faces (no familiarity). Faces to be studied (previously unknown) were presented as victims of murders or accidents with a description provided in the form of a police dossiers featuring a short text accompanied by several pictures of the victims. This experimental manipulation was included to explore the effect of emotional memory in the episodic encoding of faces. Indeed, convergent evidence suggests that emotional events attain a privileged status in memory (LaBar & Cabeza, 2006) and that memory tends to be better for emotionally arousing information than for neutral information (Buchanan & Lovallo, 2001). The reason for this potentiation has been explained by neuroscientific studies providing evidence of a more intense brain activity during coding of emotional information. For example, Mueller and Pizzagalli (2016) have provided direct electrophysiological evidence (via intracranial recordings) that faces that had been fear-conditioned (to become threatening stimuli) evoke increased activity in or in proximity of the left fusiform gyrus as early as 80 ms post-stimulus after presentation. The effect was visible starting from the same day of conditioning and, remarkably, it was still very strong one year after the fear-conditioning. In another experiment Proverbio, LaMastra, and Zani (2016) investigated the effect of social prejudice on memory for faces, by presenting hundreds of faces of male and female individuals in association with a derogatory or an appreciative description, and found that faces associated with a negative (vs. positive) prejudice elicited larger anterior negativities during encoding, smaller FN400s and larger LPs during recollection. The larger potentials for negatively-valenced faces were associated to increased activations of the limbic and parahippocampal areas.

Based on previous ERP literature, we predicted a significant modulation of FN400 and LP components as a function of stimulus familiarity (known vs. unknown). Both processes are thought to be related to two spatiotemporally different ERP effects (FN400 and LP), namely the early mid-frontal negativity (familiarity) and the late parietal old/new effect (recollection) (Evans and Wilding, 2012, Hoppstädter et al., 2015, Rugg et al., 1996, Wilding and Rugg, 1996, Wilding and Sharpe, 2003).

We sought also to investigate the impact of emotional valence on the remembering of recent faces, in the hypothesis that the threatening learning context of recently faces might made them equally memorable than robustly coded information (i.e., popular faces). Had this been the case we would have expected to find equally large FN400 responses to recent and old faces. Furthermore, we also expected a modulation of an earlier familiarity-related response (anterior N200) recently found to precede FN400 effects, and to be larger to unknown than familiar items (Lawson et al., 2012).

Additionally we also wished to investigate whether face sex significantly affected memory recollection. Indeed previous research on emotions and empathic resonance mechanisms showed that some specific factors can facilitate emotional mirroring, like perceived similarity (e.g., sex of viewer); it would influence empathic responding through the tendency to identify more closely with others who appear as being more similar in features such as personality (Gruen & Mendelsohn, 1986) or appearance (Bufalari, Porciello, Sperduti, & Minio-Paluello, 2015). On the basis of this literature (Proverbio, Riva, Martin, & Zani, 2010) we predicted a better recall of own-sex faces, sharing sexual gender with the viewer.