Conserved features of anterior cingulate networks support observational learning across species

Abstract

The ability to observe, interpret, and learn behaviors and emotions from conspecifics is crucial for survival, as it bypasses direct experience to avoid potential dangers and maximize rewards and benefits. The anterior cingulate cortex (ACC) and its extended neural connections are emerging as important networks for the detection, encoding, and interpretation of social signals during observational learning. Evidence from rodents and primates (including humans) suggests that the social interactions that occur while individuals are exposed to important information in their environment lead to transfer of information across individuals that promotes adaptive behaviors in the form of either social affiliation, alertness, or avoidance. In this review, we first showcase anatomical and functional connections of the ACC in primates and rodents that contribute to the perception of social signals. We then discuss species-specific cognitive and social functions of the ACC and differentiate between neural activity related to 'self' and 'other', extending into the difference between social signals received and processed by the self, versus observing social interactions among others. We next describe behavioral and neural events that contribute to social learning via observation. Finally, we discuss some of the neural mechanisms underlying observational learning within the ACC and its extended network.

Keywords: Amygdala; Anterior cingulate cortex; Empathy; Facial expression; Fear conditioning by proxy; Fear learning; Prefrontal cortex; Primates; Rodents; Social cues; Social dominance; Social learning; Social transmission; Vicarious learning.

Fig. 1.. Brain regions constituting the ACC in primates and rodents.

Diagrams represent midsagittal sections of the human, monkey, rat, and mouse brains, and illustrate distinct brain regions that form part of the anterior cingulate cortex. While the construction of these diagrams considered various previous studies and brain atlases (Bush et al., 2000; Paxinos and Franklin, 2019; Paxinos and Watson, 2014; Rushworth et al., 2004; Vogt and Paxinos, 2014), the sizes and boundaries illustrated for each brain region are not precise. Numerical labels represent Brodmann nomenclature, whereas alphabetical labels represent other definitions given to some of the regions in rodents. ACC, anterior cingulate cortex; MCC, mid anterior cingulate cortex; Cg1, cingulate area 1; Cg2, cingulate area 2; PL, prelimbic cortex; IL, infralimbic cortex; CC, corpus callosum.

Fig. 2.. ACC connectivity in rodents is organized to integrate complex sensory, cognitive, and emotional information.

Left, Schematic of cortical layers in the rodent ACC. Cortical layers are color-coded. CC stands for corpus callosum. Right, Summary of connections of individual ACC layers with other brain areas involved in sensation, cognition, affect/arousal, and neuromodulation, based on anatomical tracing and electrophysiology studies (Aston-Jones and Waterhouse, 2016; Bissière et al., 2008; Cruikshank et al., 2012; Gabbott et al., 2005; Hoover and Vertes, 2007; Kamigaki, 2018; Lee et al., 2005; Little and Carter, 2012; Sara and Hervé-Minvielle, 1995; Vertes, 2004). Thicker and thinner arrows represent stronger and weaker connections, respectively. While stronger sensory inputs to the ACC tend to arrive through the supragranular layers 2/3, and stronger outputs originate in the infragranular layer 5, cells in both supragranular and infragranular layers also form extensive reciprocal connections with many brain areas involved in sensation, cognition, affect/arousal, and neuromodulation. The strong reciprocal connectivity of the ACC with this extended network may be optimal for integrating different types of information, including social and environmental cues, to facilitate observational learning.

Fig. 3.. Activity in the ACC-BLA pathway during observational fear conditioning. Illustrations summarize findings by Allsop et al. (2018).

A, Schematic of the observational fear paradigm. Demonstrator mice received tone-shock pairings, while observer mice witnessed these events through a transparent wall from the adjacent compartment. B, Schematic of in vivo neural recordings combined with optogenetic strategies to monitor the activity of either ACC-to-BLA projectors or BLA neurons during the task. C, ACC-to-BLA projectors acquired prominent responses to the shock-predicting cue. D, BLA neurons also acquired prominent responses to the cue, but such responses were abolished by photoinhibition of the ACC input.