The Vertebrate mesolimbic reward system and social behavior network: A comparative synthesis

Abstract

All animals evaluate the salience of external stimuli and integrate them with internal physiological information into adaptive behavior. Natural and sexual selection impinge on these processes, yet our understanding of behavioral decision-making mechanisms and their evolution is still very limited. Insights from mammals indicate that two neural circuits are of crucial importance in this context: the social behavior network and the mesolimbic reward system. Here we review evidence from neurochemical, tract-tracing, developmental, and functional lesion/stimulation studies that delineates homology relationships for most of the nodes of these two circuits across the five major vertebrate lineages: mammals, birds, reptiles, amphibians, and teleost fish. We provide for the first time a comprehensive comparative analysis of the two neural circuits and conclude that they were already present in early vertebrates. We also propose that these circuits form a larger social decision-making (SDM) network that regulates adaptive behavior. Our synthesis thus provides an important foundation for understanding the evolution of the neural mechanisms underlying reward processing and behavioral regulation. J. Comp. Neurol. 519:3599-3639, 2011. INDEXING TERMS: social behavior; comparative neuroanatomy; amphibian; reptile; bird; teleost; reward system; social behavior network; limbic system; neural circuitsThroughout their lives, all animals constantly face situations that provide either challenges (e.g., aggression, predation) or opportunities (e.g., reproduction, foraging, habitat selection) (for a detailed review, see O'Connell and Hofmann, 2011). In all cases, environmental cues are processed by sensory systems into a meaningful biological signal while internal physiological cues (e.g., condition, maturity) and prior experience are integrated at the same time. This process usually results in behavioral actions that are adaptive, i.e., beneficial to the animal. To accomplish this, an animal's nervous system must evaluate the salience of a stimulus and elicit a context-appropriate behavioral response. Despite tremendous progress in understanding the ecology and evolution of social behavior (Lorenz, 1952;Tinbergen, 1963;Lehrman, 1965;von Frisch, 1967;Krebs and Davies, 1993;Stephens, 2008), it is less understood where in the brain these decisions (e.g., about mate choice or territory defense) are made and how these brain circuits have arisen over the course of vertebrate evolution.Recent research has begun to decipher the neural basis of social decision-making. In mammals in particular, the neural circuits that evaluate stimulus salience and/or regulate social behavior have been uncovered to some degree: the mesolimbic reward system and social behavior network (Fig. 1). It is becoming increasingly clear that the reward system (including but not limited to the midbrain dopaminergic system) is the neural circuit where the salience of an external stimulus is evaluated (Deco and Rolls, 2005;Wickens et al., 2007), as appetitive beh...

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

“…11); this is a measure of the degree to which nodes correlate with multiple modules and has been argued to be an appropriate measure of "hubness" for correlation-based networks 73 . Agranular insular (AI) cortex was among the nodes with the highest participation coefficients along with prelimbic prefrontal cortex (PL), piriform cortex (Pir) and dorsal bed nucleus (BSTd), regions that are associated with emotion contagion 52 , social learning 74 and social decision-making 6 , respectively. Thus, datadriven network analyses revealed functional integration among regions in the social brain, and that the insula is positioned to interact with previously identified nodes important for social and affective behaviors.…”

“…Sensory and perceptive systems in the "social decision-making network" (SDMN) which consists of the social brain network 4 and the mesolimbic reward system 5 allow one to appraise these social stimuli and integrate them with past experiences, situational, and somatic factors to shape specific behavioral responses 6 . In addition to the SDMN, growing evidence implicates insular cortex in responding to socioemotional stimuli in humans.…”

Social information changes the brain

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Sexual attractiveness: a comparative approach of morphological, behavioral neurophysiological signaling in women and nonhuman primate females

“…The main buain stuuctuues of the mesolimbic uewaud system aue the stuiatum (STR: compulsive behaviou), ventual tegmental auea (VTA: motivation, uepuoduction, pauental caue), medial amygdala (meAMY: agguession uepuoduction, pauental caue, social uecognition), ventual pallidum (VP: emotional leauning, pauental behaviou), nucleus accumbens (NAcc: emotional leauning, impulsivity, motivation, pauental caue), and the hippocampus (HIP: spatial leauning) (behavious fuom O'Connell & Hofmann, 2011;Beuuidge & Kuingelbach, 2008). In humans the subcoutical cognition and coutical consciousness of pleasuue is uelated to activity uates in the medial oubitofuontal, mid insulau, and the anteuiou cingulate aueas (de Auaujo et al, 2003).…”

“…Inteuestingly, both buain aueas, the social behaviou netwouk and the uewaud system, consists of highly inteuactive nodes and oveulapping stuuctuues, which uepuesent an integuated evolutionauy ancient social decision-making netwouk (O'Connell and Hofmann, 2011).…”