The brain's relevance detection network operates independently of stimulus modality

Abstract

Brain regions associated with the processing of emotional stimuli are often also associated with the processing of social stimuli. Therefore, this network consisting of the amygdala, the anterior insula, the superior temporal sulcus (STS), and the orbitofrontal cortex (OFC) may rather be involved in more general relevance detection which should be independent of the sensory modality of the stimuli. In the current study, we used functional MRI to measure brain activations while participants either viewed pictures that varied in their emotional and social content or listened to sounds that varied along the same dimensions. The amygdala, the anterior insula, the STS, and the OFC showed increased activation during processing of emotional as well as social stimuli independent of the sensory modality in which the stimuli were presented. Moreover, social emotional stimuli elicited more pronounced activity in this network than stimuli with solely emotional or social content. These results indicate that the proposed network involved in relevance detection works independently of the source of relevance (emotional or social information mediated by the stimulus) and modality.

Introduction

One of the most important functions of the human brain is to register and selectively respond to those stimuli in the environment that are of significance for the organism. Stimulus significance can be determined by stimulus features such as intensity or novelty, but also by their emotional relevance, e.g. being capable to elicit an emotional response. Moreover, emotionally evocative stimuli often also have a social reference [8], [24]. Socially generated emotional stimuli motivate people to act in social interactions, e.g. a smile stimulates a smile, a verbal attack provokes a defensive or aggressive response and the hope of a future social incentive, e.g. to get a promotion, increases the effort put into work. This interpersonal character of emotions gained more and more attention in recent years. Emotions help to coordinate social interactions through their informative, evocative, and incentive functions [16]. Thus, one could argue that brain areas critical for processing of emotionally relevant stimuli might also be involved in the processing of the social relevance of external stimuli.

Adolphs and Spezio proposed a neural network for social cognition including cortical (e.g. the orbitofrontal cortex (OFC) and the primary visual cortex) and limbic structures (e.g. the amygdala and the insula), that are also critically involved during processing of emotionally relevant stimuli [1]. According to this model, the amygdala plays a critical role in this network as it modulates the activity in other parts of the network [35], [38]. Increased activation of the amygdala has reliably been found during processing of both unpleasant (including fear evoking) and pleasant stimuli in numerous functional brain imaging studies [9], [11], [20], [27], [37]. Moreover, increased activation of the amygdala has also been found during social cognition, e.g. during processing of emotional facial expressions [7], [36], in the evaluation of trustworthiness in faces of unknown people [2], [39] and in the processing of novel neutral faces compared to repeatedly shown neutral faces [40]. These data suggest that the amygdala is involved in more general relevance detection rather than specifically in emotion processing (cf. [29]). The amygdala not only has connections to subcortical regions including the brain stem but also to several cortical areas [3] putting this structure forward as an ideal candidate for a first stage relevance detector.

Although many studies investigated brain responses to emotional vs. neutral and to social vs. non-social stimuli only few studies explored the interaction between both dimensions. Using pleasant, neutral, and unpleasant pictures from the International Affective Picture System (IAPS [19]) divided into social (pictures that contained faces and bodies) and non-social (objects and animals) stimuli, a clear interaction between processing of social and emotional information in the STS, the middle occipito-temporal cortex, and the thalamus was observed [24]. Emotional pictures with socially relevant information evoked stronger activation in these regions than all other groups of pictures. The authors interpreted this interaction as a synergistic effect of social and emotional cues grabbing more natural selective attention [18]. In contrast, the amygdala was activated additively, not interactively, by social and emotional information, supporting the hypotheses that the amygdala appears to be primarily involved in relevance detection, regardless of the nature of the relevance (i.e. social or emotional relevance). Another study [8] combined film clips with static pictures varying along the social and the emotion (valence) dimension. Amygdala activity was associated with both dimensions, while only the social emotions (joy and sadness) activated the superior temporal gyrus. Therefore, both studies clearly underscore that those brain regions involved in the processing of emotional stimuli are also modulated by the social relevance of these cues, either interactively or additively. In the current study, we extended this work by using both visual and auditory stimuli and investigated the effect of social information embedded within emotionally evocative stimuli.

Functional brain imaging studies also reported increased amygdala activation to emotional human sounds [15], [30]. Enhanced responses to emotional vocalizations were also found in the anterior insula [23] and the prefrontal cortex [12]. In addition, emotional compared to neutral prosody was found to elicit increased responses in voice specific areas of the middle superior temporal sulcus [14]. Thus, significant auditory stimuli seem to be processed in the same neural networks that are described by the model of Adolphs and Spezio developed for visual stimuli [1]. The first study that compared brain responses to both visual and auditory emotional stimuli found increased amygdala activation to emotional pictures and sounds [4]. The current study follows up on this research and subdivided emotional and neutral visual and auditory stimuli into those that convey social information and those which do not. If the neural networks described above are indeed specialized for extracting emotionally and socially relevant information from the environment, this capacity should be independent of the sensory modality of the stimuli.