Incidental learning of faces during threat: No evidence for enhanced physiological responses to former threat identities

Humans have difficulties in identifying unfamiliar persons, especially when the situational context changed (Davies and Milne, 1982, Burton and Jenkins, 2011, Young and Burton, 2017). This can become dangerous, e.g., when a person encountered in a hostile situation is met again but not recognized. During initial encounter, defensive response programs are activated when an evolutionary prepared aversive situation occurs (e.g., fear, freezing, fight/flight; Öhman & Mineka, 2001). In the second encounter, when the unfamiliar person is not identified, the aversive context of the first encounter is hardly recognized at all (Arnold et al., 2021). However, the question remains whether the unrecognized person is nevertheless associated with the threatening context even though neither is remembered. Thus, the present research question is whether we find defense activation (i.e., enhanced skin conductance response [SCR] and startle reflex) to non-recognized faces that were previously encountered in a threatening context.

Psychophysiological defense mechanisms have been hypothesized to function relatively independently of conscious cognitive processing of stimulus associations (e.g., Carretié et al., 2009, Öhman and Mineka, 2001). For instance, on the neural level, a recent study observed selective processing of previously seen faces as a function of whether faces were encoded in a threatening or safe context (Schellhaas et al., 2020), and this effect was replicated in individuals with adverse childhood experiences (Schellhaas et al., 2022). Intriguingly, this differential old/new-ERP effect was not reflected in conscious recognition performance in either study and resulted in poor face and context memory. Such difficulties in recognizing unfamiliar faces seen only briefly (e.g., for 1s or 6s) have also been observed in other studies in which a large number of ninety faces were presented in a blocked manner (Arnold et al., 2021). Participants did not know whether and, possibly more importantly, under what conditions they had seen a person before (i.e., during threat or safe conditions). Because neural processing is assumed to have direct access to defensive response programs irrespective of conscious face and context recognition (e.g., Carretié et al., 2009) the question emerged whether threat-selective perceptual processing results in priming of defensive psychophysiological response patterns to unrecognized threat relative to safety associated faces.

From a clinical perspective this is an important question as perceptual biases and physiological arousal may contribute to threat-associated identity recognition deficits in (socially) anxious and/or traumatized participants (Ehlers & Clark, 2000). In this context, recent research suggested attentional threat biases and hypervigilance for highly anxious individuals (Shackman et al., 2016, Robinson et al., 2012). Moreover, the generalization of the defensive startle reflex activity is a central feature of pathological anxiety especially for posttraumatic stress disorders (Dunsmoor and Paz, 2015, Lissek et al., 2008, McTeague and Lang, 2012, Lang and McTeague, 2009). However, it is not clear to what extent threat-induced overgeneralization and attentional biases extend to memory processes and remain constant once the acute threat has disappeared. Here, recent studies found episodic memory to be facilitated through Pavlovian threat-conditioning procedures following a period of consolidation but not in an immediate memory test (Dunsmoor et al., 2015, Kroes et al., 2017, Starita et al., 2019). Moreover, episodic memories for threatening events generalize after an aversive conditioning procedure (Starita et al., 2019). An adaptive bias toward threat thus manifests in memory to avoid potential future harm after the actual experience of threat. However, it is unclear whether these biases extend to the effects of social threat learning, in which actual threat is not directly experienced but modeled by aversive expectation. Furthermore, it remains an open question whether an immediate memory test leads to enhanced neural processing (Schellhaas et al., 2022, 2020) and triggers or prevents a psychophysiological response to threat identities that have not yet been consolidated.

The present study examined whether participants show threat-enhanced physiological responses (i.e., enhanced SCRs and threat-potentiated startle reflex) to faces that were previously met in a threat context but cannot be remembered. To this end, an item/source (i.e., face/context) recognition task was combined with the threat-of-shock paradigm, in which participants were verbally informed about the possibility to receive electrical shocks when a particular colored background was present (e.g., blue signals threat) whereas another background color indicated safety (e.g., green signals safety). During an initial encoding phase (incidental learning), unfamiliar faces were paired with either a threat or safety context. It is assumed that defensive responses are increased for faces in a threat relative to a safe context (i.e., threat-potentiated startle and SCR; Grillon and Charney, 2011, Bublatzky et al., 2013). Moreover, startle potentiation should be more pronounced in more (socially) anxious participants while the difference between threat and safety decreases (generalization, Lissek et al., 2008, Lobo et al., 2015).

During the following recognition phase, an unexpected item/source recognition task was performed. Participants indicated whether they had seen a face with a threat or safety background, or whether it was new. Despite the notion of a memory enhancing effect of aversive apprehension (Dolcos et al., 2012, Ventura-Bort et al., 2016), we expected rather poor recognition performance for incidentally learned faces as in our previous studies (Arnold et al., 2021, Schellhaas et al., 2020, Schellhaas et al., 2022; see for a more general review Burton & Jenkins, 2011). Of particular interest is the physiological responding to faces that had been seen previously within threat compared to safety background. According to the notion of a threat advantage (Öhman & Mineka, 2001), faces encoded during threat should elicit enhanced SCRs and startle reflex potentiation during recognition relative to safely encoded faces (Dunsmoor et al., 2015, Starita et al., 2019). Similar to encoding, more pronounced SCRs and startle reflex are expected for (socially) anxious (Wangelin et al., 2012) and traumatized participants with more severe anxiety (Lobo et al., 2015). For these participants, less face differentiation (old-threat vs. old-safe vs. new) was expected, reflecting maladaptive evaluative processing of threatening face–context compounds.

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