Compassion and admiration: Neural reuse between a social and a somatosensory system

A growing body of evidence points to developmental and evolutionary reuse between a social and a somatosensory system in the feeling of social emotions. Brain systems involved in the direct sensation of physical pain in the gut and viscera (e.g., during stomach ache), are also involved in the feeling of one's own social or psychological pain (Decety & Chaminade Reference Decety and Chaminade2003; Eisenberger & Lieberman Reference Eisenberger and Lieberman2004; Panksepp Reference Panksepp2005). These systems are also involved in the feeling of late-developing social emotions about another person's psychologically or physically painful, or admirable, circumstances (Immordino-Yang et al. Reference Immordino-Yang, McColl, Damasio and Damasio2009). These systems most notably involve the anterior insula, anterior middle cingulate, and ascending somatosensory systems in the dorsal midbrain, most directly associated with regulation of arousal and homeostasis.

Comparative social status: Neural reuse between a social and a cognitive system

The intraparietal sulcus (IPS) is important in representing comparative numerosity, quantity, magnitude, extent, and intensity (Cohen et al. Reference Cohen Kadosh, Lammertyn and Izard2008; Dehaene et al. Reference Dehaene, Piazza, Pinel and Cohen2003); it is also involved in representing social status hierarchy (Chiao et al. Reference Chiao, Harada, Oby, Li, Parrish and Bridge2009b). Particularly when comparisons are close, neural activations observed within the IPS for numerical and social status comparisons parallel behavioral distance effects in reaction time and error rates, and are thought to reflect a domain-independent spatial representation of magnitude, including the “magnitude” of social rank.

All animals are responsive to magnitudes, distances, temporal intervals, and intensities (Gallistel Reference Gallistel1993). The neurocognitive systems that support this seem to have been reused in evolution to represent the linear dominance hierarchies that are ubiquitous in both vertebrates and invertebrates. Social dominance hierarchies existed long before the invention of symbols to mediate mathematical calculation, so it is likely that the neural systems modern humans use for analog processing of numerical symbols reflect this phylogenetic history.

The social chicken or the useful egg? Learning cognitive skills through cultural transmission

In addition to demonstrating neural reuse in the social brain, the juxtaposition of these examples demonstrates the importance of considering the social sources and functions of the complex skills underlain by neural reuse. Many of modern humans' complex mental functions, both social and nonsocial, are learned through cultural transmission of practices and cognitive techniques, and are further shaped by social values, emotional relevance, and cultural modes of thought. For example, the use of numeral symbols to represent, remember, and communicate magnitude depends on the cultural invention and transmission of such symbols. Learning to use a number board or abacus allows the reuse of systems in the motor and visual cortices to calculate and remember quantities. Similarly, the cultural invention and transmission of calendars and later digital PDAs entails the reuse of perceptual object recognition and spatial relations systems, in conjunction with fine motor control skills, for temporal mnemonics. Similar processes operate in neurochemistry. For example, oxytocin, whose original functions were to mediate birth and lactation, was evolutionarily reused to bond infants and mothers, then further reused in a small proportion of mammals for parental pair-bonding (Lee et al. Reference Lee, Macbeth, Pagani and Young2009). Subsequently, oxytocin systems were culturally reused in diverse social bonding rituals and recently exploited in recreational ingestion of MDMA (ecstasy).

The function of culture in shaping the use of neural systems is demonstrated by cultural variation in the neural correlates of visual attention (Lin et al. Reference Lin, Lin and Han2008) and self-representation (Chiao et al. Reference Chiao, Harada, Komeda, Li, Mano, Saito, Parrish, Sadato and Iidaka2009a), including differential activation patterns within the same neural systems, which can be manipulated by cultural priming in bicultural individuals (Chiao et al. Reference Chiao, Harada, Komeda, Li, Mano, Saito, Parrish, Sadato and Iidaka2010). Together, these findings suggest that Anderson's assertion that putting “together the same parts in the same way [will lead to] the same functional outcomes” (sect. 1.1, para. 6) may not adequately account for the dynamic effects of socialization on neural reuse.

Conversely, the reuse of a neural system for a more complex, culturally organized task apparently can affect its recruitment for a phylogenetically or ontogenetically earlier use. Cross-cultural psychiatric research shows that various Asian populations tend to manifest psychosocial distress somatically, in medically unexplained bodily symptoms, whereas Westerners tend to express depression psychologically (Parker et al. Reference Parker, Cheah and Roy2001). Cross-cultural work in progress by Immordino-Yang and colleagues suggests that such tendencies may be associated with cultural differences in the recruitment of neural systems for somatosensation in the cortex and brain stem during social processing, extending even into midbrain nuclei that regulate basic bodily functions.

From use to reuse and back: Toward a dynamic, sociocultural theory of reuse

Anderson's theory proposes that neural reuse is mainly a process of organizing low-level circuits with relatively fixed functions into interconnected networks, and that functional differences between cognitive domains correspond to differences in the architecture or organization of these networks. Here, we argue that Anderson's model should be expanded to account for the possibilities that social learning produces distinct culturally informed operations within architecturally similar complex networks, and that the reuse of a low-level neural circuit may, in turn, influence its original, primary function. Future research should investigate how socioculturally shaped ontogenetic processes interact with the constraints and potentials of neural subsystems, connectivity, and chemistry. Are there (as Anderson assumes) fundamental components of neurocognition that are not decomposable – or how modifiable are the functions of such basic components? What biologically and culturally transmitted processes, and what social and nonsocial experiences at what stages of development, determine how neurocognitive components are combined? In humans, neural reuse involves dynamic interplay among social and nonsocial (re)uses over developmental, cultural-historical, and evolutionary timescales.