Toward a neural basis for social behavior

Abstract

Nearly 25 years ago, the shared interests of psychologists and biologists in understanding the neural basis of social behavior led to the inception of social neuroscience. In the past decade, this field has exploded, in large part due to the infusion of studies that use fMRI. At the same time, tensions have arisen about how to prioritize a diverse range of questions and about the authority of neurobiological data in answering them. The field is now poised to tackle some of the most interesting and important questions about human and animal behavior but at the same time faces uncertainty about how to achieve focus in its research and cohesion among the scientists who tackle it. The next 25 years offer the opportunity to alleviate some of these growing pains, as well as the challenge of answering large questions that encompass the nature and bounds of diverse social interactions (in humans, including interactions through the internet); how to characterize, and treat, social dysfunction in psychiatric illness; and how to compare social cognition in humans with that in other animals.

Figure 1. What Is Social Neuroscience?

(A) Metrics of publications over the years. Left: The graph plots the proportion of publications in social neuroscience relative to those in all of neuroscience, using Web of Science and methodology described in Matusall et al. (2011) (updated). Right: Past and current emphases in social neuroscience, obtained by mapping publications in social neuroscience onto the topics shown (see Matusall et al., 2011 for details). (B) How important to social neuroscience are four major themes (differently colored rows)? The figure shows histograms of the distribution of online responses obtained from ca. 85 members of the Society for Social and Affective Neuroscience (SANS) and the Society for Social Neuroscience (S4SN). (C) The methods (in rank order) used by social neuroscientists; data from the same respondents as in (B). Abbreviations are as follows: functional magnetic resonance imaging (fMRI), electroencephalography (EEG), magnetic resonance imaging (MRI), transcranial magnetic stimulation (TMS), near infrared spectroscopy (NIRS), positron emission tomography (PET), and magnetoencephalography (MEG).

Figure 2. Three Views of the Social Brain

(A) The original view elaborated a set of brain structures originally proposed by Leslie Brothers (Brothers, 1990). (B) The current view ties subsets of these structures together into functional networks that subserve particular components of social cognition; both (A) and (B) are from Kennedy and Adolphs (2012). (C) Hints of a future view in which brain networks are derived by mining large data sets (NeuroSynth; Yarkoni et al., 2011). Left: Lateral (top) and medial (bottom) views of a reverse-inference map (generated using 293 studies) indicate the likelihood that the term “social” was used in a study given the presence of activation, i.e., p(term|activation) (brain activity displayed using NeuroLens; http://www.neurolens.org). We compared this map to that of 200 independently identified Topic maps (Yarkoni et al., 2011; http://neurosynth.org) and identified those that were based on more than 30 studies and that either covered more than 50% of the “social” term map (middle) or were more than 50% covered by the “social” term map (right). Topic 116 was primarily concerned with emotion; Topic 135 with social games and interactions; Topic 143 with mentalizing; Topic 20 with fear and arousal; and Topic 30 with consciousness and awareness. Although these data-mining results should be considered preliminary, they suggest several intriguing patterns: dorsomedial prefrontal cortex appears to subserve a general role, appearing ubiquitously across the networks, whereas regions of the precuneus may be involved more selectively, distinguishing between emotion and social games. It is also interesting to observe that the amygdala is identified in all maps with the exception of Topic 143 (mentalizing). Approaches such as the example we show here should be used in future studies that make an effort to combine and reconcile data-mining results with the results of particular experimental studies.

Figure 3. A Schematic Representation of the Relative Strengths and Weaknesses of Four Animal Groups Commonly Used to Study Social Neuroscience

Relative rank ordering of the four different groups (human, nonhuman primate, rodent, and insect) for each of nine themes pertaining to social neuroscience. Darker, thicker bars indicate a higher rank order. The orderings depicted represent the authors’ sense of the field. It is the authors’ expressed opinion that no single level of study is superior to any other. Rather, all are informative and advance the cause of social neuroscience.