These results indicate that the mPFC and premotor areas might be associated, but are not crucial to EPC. However, the mPFC supports socio-cognitive skills necessary to interpret complex emotion such as inferring mental states. Additionally, the premotor cortex involvement may reflect the participation of the mirror neuron system for prosody processing particularly of complex emotion.

Emotional prosody comprehension (EPC), the ability to interpret another person's feelings by listening to their tone of voice, is crucial for effective social communication. Previous studies assessing the neural correlates of EPC have found inconsistent results, particularly regarding the involvement of the medial prefrontal cortex (mPFC). It remained unclear whether the involvement of the mPFC is linked to an increased demand in socio-cognitive components of EPC such as mental state attribution and if basic perceptual processing of EPC can be performed without the contribution of this region.

Introduction

Human everyday verbal communication involves not only semantic but also non-linguistic, information being carried by the voice [1]. This phenomenon, known as prosody, comprises acoustic features such as pitch, amplitude, segment and pause duration and allows for the encoding and decoding of emotions in speech [1], a skill which is necessary to ensure effective social communication [2].

We will denote the act of decoding emotion cues conveyed by prosody as emotional prosody comprehension (EPC). EPC does not represent a single construct. There are qualitative differences between simple emotions and more complex emotional states. Therefore, EPC is a multi-level mechanism, from the decoding of simple emotions such as fear, happiness or anger to the assessment of complex mental states. Furthermore, EPC is regarded as one of the precursor of emotional theory of mind [3]. Evolutionary, simple emotions evolved for “their adaptive value in dealing with fundamental life tasks” [4]. They are shared with other primates, include a distinctive, universal physiological response [4] and are characterized by automated and complex changes involving facial and vocal expressions [5]. They only last for a limited period of time, are highly stereotypical and involve very limited cognitive processing [5]. In contrast, complex emotions, and especially social emotions such as pride, guilt and embarrassment, require the interpretation of social intentions [6], consideration of other people, comprehension of social norms and recognition of personal responsibility for the consequences of a situation [7]. They require the monitoring of attitudes and opinions of others regarding our own behaviour, are culturally dependent, and rely upon the evaluation of others [8]. Non-social complex emotions, such as thoughtfulness, boredom or interest are belief-based rather than situation-based and reflect the inner thoughts of an individual [9]. An important difference between complex emotion and simple emotion is based on the fact that complex emotions involve adjudicating a cognitive state as well as an emotion and are context and culture dependent [10] [11]. The cognitive content is an essential constituent of the emotion and it is a relevant part of what causes the emotion [12]. Thus, complex emotions are a cognitively enriched extension of simple emotion [12] and additional cognitive elaboration is necessary to process complex mental states [13].

At the behavioural level, studies have sought to determine whether emotion comprehension for simple emotion and complex emotion is differentially affected by neurological impairments and childhood development, which might imply separate neural processes. However, findings have been equivocal. One study in children with learning disabilities revealed difficulties in understanding complex social emotions such as pride or guilt together with a preserved ability to recognize simple emotions such as happiness or sadness [7], suggesting that both emotional processes might be neuronally dissociated. In agreement with these finding, another study using facial stimuli found a similar dissociation between the comprehension of simple and complex emotion in patients with schizophrenia [14]. On the other hand, a recent study looking at the detection of sarcasm (a complex emotion) and simple emotion from vocal cues found that performances in both tasks were highly correlated in both a control and a schizophrenic patients group. [15].

Looking at functional brain imaging data, some clinical studies have indicated overlapping brain areas involved with simple and complex emotion comprehension deficits [16]–[17]. To the best of our knowledge, however, there have not yet been any studies in healthy participants which have directly compared the brain networks involved with simple and complex emotion comprehension from speech cues. Such studies might be especially interesting, as simple and complex emotion comprehension might be mediated by different brain areas, even if they appear correlated on the behavioural level. Previous neuroimaging studies have shown that, EPC in general is supported by a temporo-frontal network [18]–[21]. However, the role of each of the neural components in the network, particularly the involvement of prefrontal nodes, is still under debate.

Some authors have claimed that the involvement of prefrontal regions in EPC depends on linguistic features of the stimuli. One study [22] found that concurrent semantic content of prosodic cues resulted in increased activation of the inferior frontal gyrus, while activation of the posterior lateral temporal lobe during prosody decoding remained constant independently of the semantic load of the stimuli [21]. Interestingly, it has been suggested that increased (semantic) processing demands may therefore have little effect on the auditory cortex response, but may modulate the frontal lobe response [23]. Conversely, it has been proposed that taking away the labelling element of typical EPC tasks (such as classifying the stimuli into a category represented with a word like “happy”) and asking participants to discriminate EPC instead (make same/different judgements about the emotion conveyed in pairs of sentences) reduces frontal lobe activity [23], indicating that the demand on frontal lobe resources is reduced when EPC are reduced to purely perceptual judgements.

An alternative model of emotion perception proposes that in order to decode other persons's emotions, postural, facial or vocal cues are observed, which activate engrams to simulate a similar emotion [24]. Such an internal simulation facilitates the sensation of the emotional state in an embodied way, which then is interpreted and attributed to other individuals. If this model is correct, the recruitment of a mirror neuron system for the perception of emotions would be necessary. In fact, the role of a mirror system for emotion decoding from facial emotion [25]–[26] as well as prosody [27]–[29] have been proposed. Some of these studies suggested that the engagement of the mirror system depends on the empathic characteristic of the participants [27]. For example, in a prosody decoding task, activations in the bilateral superior, middle and inferior frontal gyri, as well as the anterior insula and bilateral perisylvian activation inversely correlated with empathic ability [27]. The extensive activation including the bilateral superior, middle and inferior frontal gyri may relate to inner simulation of the emotional state of others [30] which might be particularly crucial for more demanding emotions in which the inference of intentions is required [31]. Thus, it is plausible to predict that premotor activation would be more prominent for complex social emotions in comparison to simple.

The mirror neuron system helps to understand the mental states of other on the basis of our own mental state, which is the first step for theory of mind (ToM) [32]. It has been proposed that making inferences about social interactions (a task which requires ToM) relies upon the integrity of the orbitofrontal as well as the medial prefrontal cortex [32]–[33]. ToM skills may be particularly needed in EPC for complex and social emotion because they imply to adjudicate inner thoughts to the individual experiencing the mental state in the case of the non-social complex emotion, whereas social emotion require the interpretation of social cues, taking the dyadic relation in which the emotion emerges. If this is true, the neural network underlying ToM should also underlie EPC for complex and social emotions.

The present study examines the neural correlates of EPC of simple and complex emotion from vocal cues. This investigation proposes that EPC for both simple and complex emotion share common neural components, but additional socio-cognitive modules are recruited for complex emotion. It is hypothesised that the neural correlates of the complex emotion comprehension differ from those of simple emotion due to the requirement of taking the emotional perspective of other [33] which might partly rely on mental state decoding skills [34]. Specifically, we predict that EPC for complex emotion involves activation of the orbitofrontal and medial PFC as part of the social brain [35] as well as the premotor cortex as a part of the mirror neuron system, indicating that the involvement of the PFC in EPC depend on the complexity of social judgments involved in the task.