A deletion variant of the ADRA2B gene that codes for the α2b adrenoceptor has been linked to greater susceptibility to traumatic memory as well as attentional biases in perceptual encoding of negatively valenced stimuli. The goal of the present study was to examine whether emotional enhancements of memory associated with the ADRA2B deletion variant were predicted by encoding, as indexed by the subjectively perceived emotional salience (i.e., arousal) of events at the time of encoding. Genotyping was performed on 186 healthy young adults who rated positive, negative, and neutral scenes for level of emotional arousal and subsequently performed a surprise recognition memory task 1 week later. Experience of childhood trauma was also measured, as well as additional genetic variations associated with emotional biases and episodic memory. Results showed that subjective arousal was linked to memory accuracy and confidence for ADRA2B deletion carriers but not for non-carriers. Our results suggest that carrying the ADRA2B deletion variant enhances the relationship between arousal at encoding and subsequent memory for moderately arousing events.
There is evidence that emotionally salient events are typically remembered more vividly than everyday ones (Kensinger and Corkin, 2003 and Sharot et al., 2007a). Yet individuals differ in the degree to which emotional salience enhances memory (Hamann et al., 1999 and Todd et al., 2011) as well as in their susceptibility to intrusive memories associated with post-traumatic stress disorder (PTSD) (Yehuda & LeDoux, 2007). Individual differences may also partly explain conflicting findings in the literature, with some studies reporting that memory is enhanced for emotionally arousing relative to neutral events [e.g., (Brown and Kulik, 1977 and Ochsner, 2000)], and other studies failing to find such an effect (Sharot, Verfaellie, & Yonelinas, 2007).
The modulation hypothesis (McGaugh, 2002) proposes that increased norepinephrine (NE) activity in the basolateral amygdala (BLA) elicited by an affectively salient event enhances encoding of the event. Such arousal related activity at encoding further interacts with the influence of NE on longer-term memory consolidation processes to enhance memory for salient events (Cahill and Alkire, 2003 and Roozendaal and McGaugh, 2011). This hypothesis is supported by findings that in rats, administration of NE into the BLA both prior to and following encoding of an event is associated with enhanced memory (for review see Roozendaal et al. (2009) and Roozendaal and McGaugh (2011)). In humans, the influence of arousal on both encoding and post-encoding processes has been demonstrated by injecting epinephrine or exposing participants to emotionally arousing images prior or subsequent to encoding (Anderson et al., 2006, Cahill and Alkire, 2003, Cahill et al., 2003, Cahill et al., 1994 and Schwarze et al., 2012). We have recently shown that, in humans, enhanced arousal at encoding is associated with the experience of emotion enhanced perceptual vividness (EEV), which in turn predicts the vividness of later memory (Todd, Talmi, Schmitz, Susskind, & Anderson, 2012).
Recently a deletion variant of the ADRA2B gene, which codes for the α2b adrenoceptor, has been linked to the emotional enhancement of memory. The deletion variant, which is associated with greater extracellular NE availability ( Small, Brown, Forbes, & Liggett, 2001), predicts greater capacity for emotionally enhanced memory as well increased propensity for intrusive traumatic memory in Rwandan genocide survivors ( de Quervain et al., 2007). There is also evidence that ADRA2B genotype influences affective biases in initial encoding. Deletion carriers have been found to show greater amygdala activation when viewing negatively-valenced scenes ( Rasch et al., 2009) and enhanced perceptual encoding of negative words in comparison with non-carriers ( Todd et al., 2013). An outstanding question concerns whether the emotionally enhanced memory experienced by deletion carriers reflects the emotional enhancement of initial encoding, as the modulation hypothesis would predict. The aim of the present study was to investigate genetic influences on the relation between responses to affectively salient stimuli at encoding and in subsequent memory.
Genotyping was performed on healthy young adults who viewed positive arousing, negative arousing, and neutral scenes and rated their subjective level of emotional arousal in response to the scenes. Participants were given a surprise recognition memory task 1 week later. As episodic memory and working memory are highly correlated (Kane and Engle, 2000 and Unsworth, 2007), and personality—in particular neuroticism—has been linked to our genes of interest (Canli, 2008), working memory and personality were measured as control variables. Participants were also genotyped for additional genetic variations associated with emotional biases (5HTTLPR and COMT) and episodic memory (BDNF, KIBRA, and ApoE) [for review see ( Todd et al., 2011)]. Because genetic variations often interact with life experience to influence behavioral outcomes ( Hyde, Bogdan, & Hariri, 2011), we also measured history of trauma exposure in childhood. If NE release during encoding is related to both the experience of arousal and later expression of enhanced memory, we expected that there would be a stronger relation between subjectively rated arousal at encoding and memory for ADRA2B deletion carriers over non-carriers after controlling for relevant variables/genes. This would further suggest a mutual enhancement of encoding and post-encoding processes by the perceived affective salience of emotional events during encoding. Based on previous findings of greater amygdala response ( Rasch et al., 2009) and rapid perceptual encoding for negative images in deletion carriers ( Todd et al., in press), we expected to find an advantage for negatively arousing images.
