In The Cognitive-Emotional Brain, Pessoa (Reference Pessoa2013) highlights the interplay of emotion and cognition in the brain. When one considers the panoply of human emotions, the emotion and cognition in surprise seems an ideal test case for this interplay.

Surprise has been intensively researched since Darwin's time, perhaps because it involves this interesting mixture of emotion and cognition. Although originally conceived of as a “basic emotion” (e.g., Darwin Reference Darwin1872; Ekman & Friesen Reference Ekman and Friesen1971; Izard Reference Izard1977; Plutchik Reference Plutchik1991; Tomkins Reference Tomkins1962), more recently surprise has been reappraised more as a cognitive state because, unlike most emotions, it can either be positively or negatively valenced (Ortony & Turner Reference Ortony and Turner1990). Surprise clearly involves an emotional reaction (often accompanied by a startle response), but it also seems to service a strategic, cognitive goal, as it directs attention to explain why the surprising event occurred and learn for the future (e.g., Foster & Keane Reference Foster, Keane, Knauff, Pauen, Sebanz and Wachsmuth2013; Macedo Reference Macedo, van der Hoek, Kaminka, Lesperance, Luck and Sen2010; Maguire et al. Reference Maguire, Maguire and Keane2011; Ranganath & Rainer Reference Ranganath and Rainer2003).

Attentional models of learning suggest that when events are surprising, they collect and focus neural resources that enhance the processing of the event and drive learning (as in, for example, the Pearce-Hall model; Pearce & Hall Reference Pearce and Hall1980; see also Hayden et al Reference Hayden, Heilbronner, Pearson and Platt2011; Roesch et al. Reference Roesch, Esber, Li, Daw and Schoenbaum2012). In neural models of surprise in learning and novelty, it is predominantly suggested that surprise arises from comparative processes between what was expected to occur and what actually occurs (e.g., Hayden et al. Reference Hayden, Heilbronner, Pearson and Platt2011; Roesch et al. Reference Roesch, Esber, Li, Daw and Schoenbaum2012; Wessel et al. Reference Wessel, Danielmeier, Morton and Ullsperger2012). Many cognitive theories of surprise take a similar view – that surprising events are low probability events in the context of the event sequence, that are schema discrepant, or conflicting with previous expectations (e.g., Meyer et al. Reference Meyer, Reisenzein and Schützwohl1997; Reisenzein & Studtmann Reference Reisenzein and Studtmann2007; Schützwohl & Reisenzein Reference Schützwohl and Reisenzein1999; Teigen & Keren Reference Teigen and Keren2002; Reference Teigen and Keren2003). However, recent theories of surprise have placed a greater emphasis on the “sense-making” aspects of surprise (e.g., Foster & Keane Reference Foster, Keane, Knauff, Pauen, Sebanz and Wachsmuth2013; Kahneman & Miller Reference Kahneman and Miller1986; Maguire & Keane Reference Maguire, Keane and Son2006; Maguire et al. Reference Maguire, Maguire and Keane2011; Pezzo Reference Pezzo2003). These sense-making theories argue that surprise is fundamentally about understanding an abnormal event, about finding an explanation for the event's occurrence. For example, the recently developed metacognitive explanation-based theory of surprise (Foster & Keane, under review), proposes that the difficulty of explaining an event informs the emotional feeling of surprise.

As Pessoa discusses at a more general level, the dichotomising of systems into a dual-process model with separable mental systems consisting of automatic versus controlled processes is questionable, whereas a continuous framework seems optimal. In the phenomenon of surprise, this continuous framework is consistent with sense-making accounts that emphasise understanding, involving the mechanism of explanation, with the feeling of surprise arising from the ease/difficulty of this understanding process. Traditionally, explanation is seen as playing a role in building causal models or predictive schemas to deal with future events (Heider Reference Heider1958; Lombrozo & Carey Reference Lombrozo and Carey2006). Apart from having a predictive role when a new situation is initially encountered, however, explanation may also serve to help people decide how information should be weighted or how attention should be allocated, even as an event is occurring (Keil Reference Keil2006; see also Foster & Keane Reference Foster, Keane, Knauff, Pauen, Sebanz and Wachsmuth2013). So, for this cognitive emotion, there is a true interaction between cognition and emotion, which seem to be intrinsically linked in the experience of surprise.

This focus on the more cognitive, explanation-based treatment of surprise has yet to be fully explored at a neurological level. However, Pessoa's suggestion that the amygdala is involved in much more than “fear,” that it has novelty, salience detection, and information gathering functions, identifies it as a candidate structure playing a role in surprise. In surprise research, it has been found that functioning of the amygdala central nucleus is important in learning (e.g., Belova et al. Reference Belova, Paton, Morrison and Salzman2007; Lin & Nicolelis Reference Lin and Nicolelis2008), but it seems that the functioning of the amygdala may only be critical at the time that the surprise is initially experienced, whereas functioning of other areas, such as the cholinergic neurons in the sublenticular substantia innominate/nucleus basalis magnocellularis, are critical when that enhanced associability gained from surprise is seen in more rapid learning (Holland & Gallagher Reference Holland and Gallagher2006).

Indeed, further hints about the importance of an interplay between cognition and emotion in surprise can be gleaned from studies of two neural mechanisms involved in processes that have been linked to surprise. These are the P300, a positive-going wave in the human ERP appearing 250–500 milliseconds after a stimulus, which is thought to respond to contextual novelty, and the N400, a negative-going wave in the human ERP which peaks around 400 milliseconds post-stimulus, and which is associated with the processing of meaningful stimuli (Coulson & Kutas Reference Coulson and Kutas2001), particularly to words and pseudowords. The N400 is additionally thought to respond to stimulus novelty (for a review, see Ranganath & Rainer Reference Ranganath and Rainer2003) and is especially large in response to semantic violations. It should be noted that the P300 is sometimes split into two components, P3a and P3b; of these, the P3b appears to be more linked to surprise (e.g., Kopp & Lange Reference Kopp and Lange2013). As an example of this interplay in surprise, P300 amplitude, although responsive to contextual novelty, is also thought to be associated with “significance” (Donchin Reference Donchin1981), “information value” (Sutton et al. Reference Sutton, Braren, Zubin and John1965), and “meaning” (Johnson Reference Johnson1986), all of which are encompassed by the proposal that it is a manifestation of “context-updating” or “understanding” during interaction with the environment (Ferrari et al. Reference Ferrari, Bradley, Codispoti and Lang2010). Motivationally significant stimuli, including emotionally valent stimuli, are associated with larger P300s than motivationally insignificant or emotionally neutral stimuli (Keil et al. Reference Keil, Bradley, Hauk, Rockstroh, Elbert and Lang2002), and studies involving feedback stimuli about monetary gains or losses have shown that the P300 is sensitive to the absolute magnitude of the feedback outcome, for both gains and losses (e.g., Yeung & Sanfey Reference Yeung and Sanfey2004). These effects of subjective probability and motivational significance on P300 amplitude are modulated by the amount of attention paid to the stimulus, particularly if the subject is engaged in a secondary task that poses increasing perceptual demands (cf. Kok Reference Kok2001). So, findings for the P300 seem to reflect that it is influenced by both cognitive and emotional components.

A reduction in N400 amplitude appears to reflect ease of processing, or ease of integration after-the-fact; more colloquially, “easier understanding” (e.g., Coulson & Kutas Reference Coulson and Kutas2001; Eddy et al. Reference Eddy, Schmid and Holcomb2006; Kutas & Federmeier Reference Kutas and Federmeier2000). It has been suggested that the N400 is larger when integration is relatively more difficult (Eddy et al. Reference Eddy, Schmid and Holcomb2006). Consistent with our approach, which encompasses both the emotional and cognitive aspects of surprise as arising from a process of attempting to explain the event, it has been suggested that in joke processing, positivities (which have been argued to reflect the more emotional surprise component) and sustained negativity of the N400 (which has been proposed to index a more cognitive reinterpretation of information) can all occur within the same time window (Coulson & Kutas Reference Coulson and Kutas2001). So, again, the N400 seems to be influenced by emotional factors as well as cognitive factors, during the same time frame, reflecting the interplay of these aspects in surprise.

The target article thus opens up exciting possibilities for future work on surprise. Neuroscientific research assessing the impact of surprise still tends to treat it as merely the disconfirmation of expectations, whereas recent theories suggest that this traditional treatment is too simplistic and that surprise should instead be conceptualised more as a feeling that arises from cognitive difficulty in explaining why an event occurred (see Foster & Keane Reference Foster, Keane, Knauff, Pauen, Sebanz and Wachsmuth2013; under review). More specifically for this article, we feel that surprise could be an interesting test case for many of Pessoa's proposals, such as his discussion of the differential possibilities of the relationship between cognition and motivation, and, more generally, for his position that cognition and emotion are fundamentally linked, as we feel the interaction between the intrinsic motivational, cognitive, and emotional components may guide our behaviour both during and in response to surprising events.