Social learning in humans and other animals

Abstract

Decisions made by individuals can be influenced by what others think and do. Social learning includes a wide array of behaviors such as imitation, observational learning of novel foraging techniques, peer or parental influences on individual preferences, as well as outright teaching. These processes are believed to underlie an important part of cultural variation among human populations and may also explain intraspecific variation in behavior between geographically distinct populations of animals. Recent neurobiological studies have begun to uncover the neural basis of social learning. Here we review experimental evidence from the past few decades showing that social learning is a widespread set of skills present in multiple animal species. In mammals, the temporoparietal junction, the dorsomedial, and dorsolateral prefrontal cortex, as well as the anterior cingulate gyrus, appear to play critical roles in social learning. Birds, fish, and insects also learn from others, but the underlying neural mechanisms remain poorly understood. We discuss the evolutionary implications of these findings and highlight the importance of emerging animal models that permit precise modification of neural circuit function for elucidating the neural basis of social learning.

Keywords: DLPFC; anterior cingulate cortex; anterior cingulate gyrus; dorsolateral prefrontal cortex; learning; social; superior temporal sulcus; temporoparietal junction.

Figure 1

Socially facilitated learning occurs through a variety of mechanisms. (A) By drawing attention to a particular location or object, social cues make foraging-relevant features more salient. Such cues may or may not be intentionally delivered by the signaler. Birds commonly use flocking information to identify the location of a food patch. Image by Dan Knudson. (B) Signals released or displayed by other individuals, including approach or avoidance behaviors, facial expressions, and chemical deposits, signal the valence of the enhanced stimulus or location. Here, minnows spend more time undercover in response to a predator the initial exposure to the predator is paired with alarm substance. Bars indicate increase in time spent hiding after a training exposure to a pike with (open bars) or without (gray bars) alarm substance. Measurements are taken during exposure to pike and alarm substance, pike without alarm substance (water only), or empty tank without alarm substance, 1, 3, and 5 days after initial exposure, respectively. ^*P < 0.05; ^**P < 0.01. Figure modified with permission from (Chivers and Smith, 1994). Minnow image by Sanse, via Wikimedia Commons. (C) Although few non-human species have been found to imitate other individuals in the strict sense, the observation and performance of motor behaviors are known to activate overlapping neural circuitry. “Mirror neurons” in the frontal cortex of macaque monkeys fire both when performing a motor act and when watching another individual perform the act. This could provide a mechanism by which appropriate behavior is “primed” in a naive individual that observes a knowledgeable conspecific. Figure reproduced with permission from (Iacoboni and Dapretto, 2006). (D) In the process of active instruction, specific information is intentionally communicated to other individuals. This is known to occur in the context of the bee waggle dance, in which the travel path to a remote nectar site is signaled to other foragers in the hive. Image by J. Tautz and M. Kleinhenz, Beegroup Würzburg, via Wikimedia Commons.

Figure 2

Sensory modalities underlying social learning differ across species. In socially-facilitated food preference, rats (top) rely heavily on olfactory signals. Olfactory trails laid by conspecifics can signal what to eat and where to find it. Moreover, olfactory components from the food detected on the breath of a conspecific, causes rats to prefer the associated food, even when tested weeks later. This preference can also be elicited by pairing the food odorant with carbon disulfide, a volatile chemical found in the breath (reviewed in Galef, 2012). In contrast, primates (bottom) are heavily visual. Visual cues convey information about the food as well as about the social agent associated with the food. Social information such as kin relationship, rank, and group membership modulates the effect of social cues on food-related learning (van de Waal et al., 2013). Rat noses photo by Alexey Krasavin; rat nose photo by Robin Stjerndorff; Chocolate photo by Simon A. Eugster; Cinnamon photo by trophygeek; Vervet head photo by Wegmann, all from Wikimedia Commons. Brain photos courtesy of University of Wisconsin and Michigan State Comparative Mammalian Brain Collections. Vervet food sharing photo modified from (van de Waal et al., 2013), with permission.

Figure 3

Hypothetical roles for macaque brain areas known to be involved in social interactions, planning and perception. Social learning may involve directing attention at others or tracking their gaze. It may also involve observing their behaviors and emulating or imitating sequences of actions. Finally, some forms of social learning might rely on observing outcomes, preferences and aversion or fear. LIP, Lateral intraparietal area; STS, Superior temporal sulcus; dlPFC, Dorsolateral prefrontal cortex; ACCg, Anterior cingulate cortex gyrus.