Putting together phylogenetic and ontogenetic perspectives on empathy

Abstract

The ontogeny of human empathy is better understood with reference to the evolutionary history of the social brain. Empathy has deep evolutionary, biochemical, and neurological underpinnings. Even the most advanced forms of empathy in humans are built on more basic forms and remain connected to core mechanisms associated with affective communication, social attachment, and parental care. In this paper, we argue that it is essential to consider empathy within a neurodevelopmental framework that recognizes both the continuities and changes in socioemotional understanding from infancy to adulthood. We bring together neuroevolutionary and developmental perspectives on the information processing and neural mechanisms underlying empathy and caring, and show that they are grounded in multiple interacting systems and processes. Moreover, empathy in humans is assisted by other abstract and domain-general high-level cognitive abilities such as executive functions, mentalizing and language, as well as the ability to differentiate another's mental states from one's own, which expand the range of behaviors that can be driven by empathy.

Fig. 1

Human empathy subsumes a number of interacting and partially dissociable neurobiological systems each having a unique evolutionary history. The interaction between emotional awareness, empathic concern and affective arousal operate on a series of nested evolutionary processes, which are intertwined with social, contextual and motivational contingencies. While empathic understanding, which encompasses self/other awareness, is probably specific to humans, empathic arousal and empathic concern are shared in common with other primates and mammals. Thus human empathy depends on ancient systems for intersubjectivity, rooted in attachment to kin and care for their well-being. However, layered on top of this, the cognitive abilities that are unique to our species – language, meta-representation and executive function – interact with more ancient systems and expand the range of behaviors that can be driven by empathy.

Fig. 2

The orbitofrontal cortex and its role in empathy. On the left, a brief summary of two inter-related neural circuits and their contribution to the processing of affective information (Hurliman et al., 2005). On the right, the shift in neuro-hemodynamic activation in the ventromedial prefrontal cortex across age in 57 participants aged from 7 to 40 years when they are shown video clips depicting an individual being intentionally injured by another. A significant negative correlation (r = −43, p < 0.001) between age and degree of activation was detected in the medial portion of the orbitofrontal cortex (x 10, y 50, z −2), while a significant positive correlation (r = 0.34, p < 0.01) was found in the lateral portion of the orbitofrontal cortex (x 38, y 48, z −8). Interestingly, the spatial organization of neurons (spacing distance in minicolumns) in this region of the prefrontal cortex differs significantly between humans and apes, and this unique increase in the distance between minicolumns takes place after the age of 2 (Semendeferi et al., 2010).

Fig. 3

Intention understanding and neural processing of others’ distress. When children (age between 7 and 11 years) are shown short video clips (2.2 s) depicting harmful situations that occur accidentally and non intentionally (like in A), the neural regions involved in processing nociceptive/aversive information such as the anterior midcingulate cortex (aMCC), anterior insula (not shown), thalamus, somatosensory cortex (not shown), supplementary motor area (SMA) and periaqueductal gray (PAG) are activated (B). When the videos depict harmful actions intentionally done by another individual (C), in addition to the network that processes aversive information, neuro-hemodynamic signal increase is detected in the amygdala (not shown), medial prefrontal cortex (mPFC) and orbitofrontal cortex (OFC) (D). Besides, both mPFC and OFC increase their effective connectivity with the fronto-parietal attention network (E), which consists of the superior precentral sulcus (PrC), superior inraparietal sulcus (IPS) and the temporo-parietal junction (TPJ). This network plays a critical role in reorienting attention to salient stimuli in the environment and is functionally connected with the neural system underpinning mentalizing (Corbetta and Shulman, 2002).

Fig. 4

Schematic illustration of the macro information processing components involved in development of human empathy. These different components are intertwined and contribute to different aspects of the experience of empathy. They feed both forward to other stages of processing thereby enhancing flexible and appropriate behavioral responses. These components are continuously and mutually influential in the course of emotion responding and are contextually embedded. 1 – Affective arousal is the first component in place in development. It has evolved to differentiate hostile from hospitable stimuli and organize adaptive responses to these stimuli. This component refers to the automatic discrimination of a stimulus – or features of a stimulus – as appetitive or aversive, hostile or hospitable, pleasant or unpleasant, threatening or nurturing. Subcortical circuits including brainstem, amygdala, hypothalamus, hippocampus, striatum, and OFC are the essential neural components of affective arousal. The amygdala and OFC with reciprocal connection with the pSTS underlie rapid and prioritized processing of emotion signals. 2 – Emotion understanding develops later, and begins to be really mature around the age of 2–3. This component largely overlaps with mentalizing-like processing and draws on the mPFC, posterior superior temporal sulcus/TPJ and vmPFC as well as executive functions. Reciprocal connectivity between posterior STS and mPFC allows the child to entertain several perspectives and a decoupling mechanism between first-person and second-person information. 3 – Emotion regulation, which enables the control of emotion, affect, drive, and motivation, begins to emerge with simple forms of self-soothing and extrinsic regulation in caregiver responsiveness to the baby's emotional expressions. The dlPFC, ACC, and vmPFC through their reciprocal connections with the amygdala, hypothalamus, brainstem play a primary role in self-regulatory processes. The sympathetic-adrenomedullary (SAM) and hypothalamic–pituitary–adrenocortical (HPA) systems are centrally modulated by limbic brain circuits that involve the amygdala, hippocampus, and orbital/medial prefrontal cortex. Both SAM and HPA are functional in newborns and mature significantly during the early years in ways. 4 – Motivation to care that produces prosocial motivation arises from a set of biological mechanisms that evolved to promote parental care and attachment. The neural underpinnings are found in subcortical systems (especially the medial preoptic area, hypothalamus and striatum) as well as neuropeptides regulating attachment particularly prolactin, oxytocin, opioids, and prolactin have relevance for regulating empathic responsiveness. Emotional experience is always continuously influenced by appraisal processes. Thus empathy is not a passive affective resonance phenomenon with the emotions of others. Rather, goals, intentions, context and motivation play feed-forward functions in how emotions are perceived and experienced. From this model, it is clear that empathy and concern for others are implemented by a complex network of widely distributed, often recursively connected, interacting subcortical and cortical circuits as well as autonomic and neuroendocrine processes implicated in affiliative behaviors.