[ARTICLE] When neutral turns significant: brain dynamics of rapidly formed associations between neutral stimuli and emotional contexts – Full Text


The ability to associate neutral stimuli with motivationally relevant outcomes is an important survival strategy. In this study, we used event-related potentials (ERPs) to investigate brain dynamics of associative emotional learning when participants were confronted with multiple heterogeneous information. Participants viewed 144 different objects in the context of 144 different emotional and neutral background scenes. During each trial, neutral objects were shown in isolation and then paired with the background scene. All pairings were presented twice to compare ERPs in response to neutral objects before and after single association. After single pairing, neutral objects previously encoded in the context of emotional scenes evoked a larger P100 over occipital electrodes compared to objects that were previously paired with neutral scenes. Likewise, larger late positive potentials (LPPs) were observed over parieto-occipital electrodes (450–750 ms) for objects previously associated with emotional relative to neutral contexts. The LPP – but not P100 – enhancement was also related to subjective object/context binding. Taken together, our ERP data provide evidence for fast emotional associative learning, as reflected by heightened perceptual and sustained elaborative processing for neutral information previously encountered in emotional contexts. These findings could assist in understanding binding mechanisms in stress and anxiety, as well as in addiction and eating-related disorders.


One important survival strategy is to perceive fluctuating changes that occur in contiguous environments in order to readjust the momentary motivational relevance of incoming information. This ability allows developing flexible and adaptive responses based on the history of contingencies encountered by the individual (Miskovic & Keil, 2012). In this sense, it has been observed that a previously neutral stimulus (conditioned stimulus; CS+) continuously associated with an aversive event (unconditioned stimulus; UCS) acquires motivational relevance, compared to a neutral stimulus (CS−) unpaired with a UCS or associated with a non-emotional UCS, a process called associative learning. Traditionally, a large number of pairings between few and/or simple CS+ and a strongly aversive UCS have been used in learning paradigms to generate strong associations (Lissek et al., 2006). However, rather than single, unambiguous and/or isolated CS/UCS pairings, we are constantly confronted with multiple different events that imply associations between neutral and moderately relevant stimuli. Thus, the use of paradigms involving ‘weak’ ambiguous situations (e.g. less salient UCS, multiple complex pairings and/or few contingencies CS/UCS) would provide a better understanding of the underpinnings of associative learning (Lissek et al., 2006; Beckers et al., 2013; Steinberg et al., 2013b; Hur et al., in press). In the present study, we investigated the role of UCS heterogeneity on the formation of associations using electrophysiological correlates of associative learning for multiple neutral events paired with multiple emotional contingencies (emotional scenes).

Recent studies from Junghöfer and colleagues (e.g. Pastor et al., 2015; see Steinberg et al., 2013b, for review) used the so-called MultiCS conditioning, in which multiple CSs+ (e.g. pictures of different faces) were associated with emotionally relevant UCSs (e.g. aversive and appetitive sounds, electric shocks), while other CSs− remained unpaired or were associated with neutral events. Brain activation was measured using electro- and magnetoencephalography (EEG, MEG) during these conditioning procedures. After multiple pairings, CSs+ compared to CSs− evoked enhanced neural activity at prefrontal and sensory cortical regions during earlier (< 300 ms; Bröckelmann et al., 2011; Steinberg et al., 2012, 2013a; Rehbein et al., 2014, 2015) and later stages of processing (> 300 ms; Pastor et al., 2015), irrespective of contingency awareness. These results suggest the existence of a rather automatic learning mechanism that rapidly transfers the emotional properties of the UCS to CSs, leading to a facilitated perceptual and a more elaborated processing of the CS+.

Nevertheless, these studies have only used highly salient UCS. Therefore, it is unclear whether such associative learning processes also occur in the presence of less intense emotional events – i.e., reproducing daily interactions – or whether the formation of associations is exclusively facilitated in survival-specific contexts (Öhman & Mineka, 2001). It is also unclear whether the acquired motivational significance leading to neural response enhancement for emotion-associated stimuli occurs rapidly after one single pairing (e.g. Morel et al., 2012; Rehbein et al., 2014), or whether more than one repetition is needed to form such associations (e.g. Steinberg et al., 2012). While most of the electrophysiological conditioning studies have used aversive cues as UCS (see Miskovic & Keil, 2012, for review), it has recently been observed that pleasant information can also serve as effective, intrinsically motivating UCSs (Schacht et al., 2012; Steinberg et al., 2013a; Blechert et al., 2016; see Martin-Soelch et al., 2007, for neuroimaging findings). Both aversive and appetitive conditioning processes likely not only contribute to various disorders, such as trauma- and stress-related disorders, but also to substance abuse and eating-related disorders (e.g. Martin-Soelch et al., 2007; Pape & Pare, 2010). Thus, more evidence regarding the effect of valence on associative conditioning is needed.

In the present study, we therefore investigated brain dynamics of associative emotional learning when participants viewed neutral objects in the context of different emotionally arousing (both pleasant and unpleasant) and neutral background scenes. Object and scene presentation occurred always in the same order; first objects were presented in isolation (CS) and then a picture scene was added as background (see Fig. 1). Pairings were presented in two consecutive blocks, allowing to compare the processing of CS+ objects – paired with emotional scenes – and CS− objects – paired with neutral scenes, before (first block) and after single pairing (second block). Based on previous EEG and MEG conditioning studies (see Miskovic & Keil, 2012, for review), we predicted enhanced processing of neutral cues previously paired with emotional contexts, irrespective of valence, relative to cues previously paired with neutral contexts at different stages of processing. Because both perceptual and sustained elaborative processing have been found to be enhanced for stimuli associated with CS+, we predicted enhanced positivity for the CS+ compared with the CS− at (a) earlier (P100) and (b) later stages of processing [late positive potential (LPP)].

Figure 1. Schematic view of the stimulus presentation during the first and the second associative learning blocks. When an object was seen during the first block, the object/background association has not yet taken place, and when the object was seen in the second block, object and background scene have been associated once. [Correction added on 19 Aug 2016, after original online publication: Figure 1 has been corrected.]

Continue —> When neutral turns significant: brain dynamics of rapidly formed associations between neutral stimuli and emotional contexts – Ventura-Bort – 2016 – European Journal of Neuroscience – Wiley Online Library


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