The nucleus accumbens is involved in both the pursuit of social reward and the avoidance of social punishment
Introduction
Understanding the brain’s receptivity to social reward and social punishment has generated extensive interest recently (Falk et al., 2012, Frith and Frith, 2012, Richards et al., 2011, Rilling and Sanfey, 2011, Seymour et al., 2007, Vrtička and Vuilleumier, 2012). However, there is still a relative paucity of neurobiological research on the human motivation for obtaining social reward and avoiding social punishment. A better knowledge of the brain–behavioral mechanisms associated with the motivation for social engagement is not only imperative for understanding the biology of socially motivated behaviors, but also for comprehending the neuropsychopathology of complex disorders such as autism, social phobia and depression which are often characterized by impairments alluded to aberrant social motivation (American Psychiatric Association, 2013).
Social motivation can be described as an individual’s propensity to obtain social rewards (Chevallier, Kohls, Troiani, Brodkin, & Schultz, 2012) (e.g., approval by others), and to avoid social punishment (e.g., disapproval by others) (Buss, 1983). Research has shown that the processing of incentives like rewards and punishments can be subdivided in at least two successive phases, with anticipation of the desired outcome and the appraisal of the experienced outcome each having a unique but interrelated neural basis (Reynolds & Berridge, 2002). Specifically, the possibility of obtaining positive incentives (e.g., praise) will trigger approach behavior, while negative incentives (e.g., threat of reprimand) facilitate avoidance (reviewed in (Young, 1959)).
One prominent experimental paradigm, the monetary incentive delay task (MID), was introduced by Knutson, Westdorp, Kaiser, and Hommer (2000) to investigate the neural processing of reward and punishment with functional magnetic resonance imaging (fMRI). The MID separately assesses anticipatory versus consummatory responses to monetary incentives (i.e., monetary gain or loss), but has most recently been modified to study the processing of social stimuli as well (Kohls et al., 2011, Kohls et al., 2012, Rademacher et al., 2010, Spreckelmeyer et al., 2009). Using the incentive delay paradigm, Spreckelmeyer et al. (2009) were the first to compare blood oxygen level dependent (BOLD) signals for anticipation of social (i.e., affirmative faces) versus monetary reward in healthy participants. In line with Knutson, Adams, Fong, and Hommer (2001), Knutson, Fong, Adams, Varner, and Hommer (2001), Knutson, Taylor, Kaufman, Peterson, and Glover (2005) and animal work (Robinson, Zitzman, & Williams, 2011), cue-triggered anticipation of social and monetary gain activated the dopaminergic mesocorticolimbic reward circuitry, including ventral striatum (VS)/nucleus accumbens (Nacc), with greater VS/Nacc activity for more salient incentives (e.g., exuberant vs. mild smiles; €3 vs. €1). These findings were replicated in more recent studies (Dichter et al., 2012, Gasic et al., 2009, Kohls et al., 2012, Smith et al., 2010), suggesting that the VS/Nacc functions as a general, modality-independent mediator of reward seeking, including the motivation for obtaining social reward (Kohls, Chevallier, Troiani, & Schultz, 2012).
Threat of punishment, a well-known motivator of human social behavior (Balliet et al., 2011, Rilling and Sanfey, 2011, Seymour et al., 2007), by contrast, has not been nearly as well studied with functional neuroimaging. Thus, less is known about the neural mechanisms underlying the motivation to avoid social punishments (e.g., disapproval). Recently, however, several fMRI studies have shown that cue-induced avoidance of negative, non-social situations such as monetary loss (Carter et al., 2009, Delgado et al., 2009, Guitart-Masip et al., 2011, Kim et al., 2006, Stark et al., 2011, Tom et al., 2007), electric shocks (Jensen et al., 2003, Mobbs et al., 2009, Seymour et al., 2005) or aversive pictures (Levita, Hoskin, & Champi, 2012) activate the VS/Nacc region in a consistent fashion. Together, these findings suggest the involvement of the VS/Nacc in both appetitive (i.e., reward approach-related) and aversive (i.e., punishment avoidance-related) motivated behavior (Bromberg-Martin et al., 2010, Carlezon and Thomas, 2009, Horvitz, 2000, Ikemoto and Panksepp, 1999, Salamone, 1994). This conclusion is further supported by animal data showing that firing of dopaminergic Nacc neurons contributes to reward-seeking as well as anticipatory avoidance in response to potentially punishing events (e.g.,(Matsumoto & Hikosaka, 2009; Pennartz, Groenewegen, & Lopes da Silva, 1994; Reynolds and Berridge, 2002, Reynolds and Berridge, 2008; Schoenbaum & Setlow, 2003)). Thus, while cue-induced VS/Nacc activation has been frequently associated with the anticipation of positive stimuli like rewards (Berridge et al., 2009, Berridge and Robinson, 2003, Kohls et al., 2012), the bivalent activation pattern that has been observed suggests that the VS/Nacc is involved in encoding the motivational value of aversive and to-be-avoided stimuli as well (Reynolds & Berridge, 2002). Presumably this should also pertain to negative social stimuli such as social disapproval – or other forms of social punishment – that humans generally strive to avoid (Homans, 1958), but to date this has not been studied.
A major challenge faced by current neuroscience research on social motivation in humans is the development of fMRI-appropriate experimental paradigms that employ ecologically valid stimuli that will initiate and maintain social approach and avoidance processes (Kohls et al., 2012). One limitation of prior studies, for instance, has been the reliance on static face images to serve as social rewards (Risko, Laidlaw, Freeth, Foulsham, & Kingstone, 2012), which are, at best, only weakly rewarding (Kohls et al., 2012). By contrast, dynamic stimuli, such as video clips of positive and negative face expressions, are perceived as more natural and engaging (Blatter and Schultz, 2006, Sato and Yoshikawa, 2007), and may contribute to more robust neural activation in social brain circuitry (Fox et al., 2009, Schultz and Pilz, 2009). Moreover, non-verbal signals like body postures and gestures are important social reinforcers (Skinner, 1953), but have not been addressed in previous imaging work on social motivation. To this end, we developed a novel set of video clips of actors providing non-verbal approval as social reward and non-verbal disapproval as social punishment, presented contingent on task performance in an incentive delay task ((Knutson et al., 2000; Spreckelmeyer et al., 2009); see below for details).
Taken together, the aim of the current investigation was twofold: First, to assess whether the neural mechanisms underlying the motivation for social reward gain (i.e., approval) would also apply to avoidance of social punishment (i.e., disapproval), with a special focus on the VS/Nacc; and second, to improve upon earlier studies by using dynamic video stimuli instead of static pictures as social incentives. We hypothesized that both the anticipation of social approval and avoidable social disapproval would activate the VS/Nacc in healthy adults.
Section snippets
Subjects
Study participants were recruited from the University of Pennsylvania graduate and undergraduate student community through flyers and word-of-mouth advertising. The initial sample consisted of 30 right-handed healthy volunteers with normal or corrected-to-normal vision. Data from five participants were incomplete and could not be used for data analyses (e.g., missing logfiles). Subsequently, three participants were excluded because of excessive head movements during the fMRI scan (i.e., more
Behavioral task performance
RT for hits were analyzed using a repeated-measures ANOVA with task (APR, AVOI) and trial (incentive, control) as the within-subjects factor in order to compare the incentive trials to the control trials within each task and across tasks. This analysis revealed a main effect of trial (F(1,21)=22.83, p<0.001, η2p=0.52), with faster RTs observed for incentive conditions relative to the neutral control condition (ps≤0.05), suggesting that incentive manipulations within the experimental tasks were
Discussion
In the present study using a newly developed set of ecologically valid social stimuli (i.e., video clips instead of static pictures), we could demonstrate that the anticipation of social punishment avoidance (i.e., disapproval) recruited the VS/Nacc circuitry in a manner that was similar to VS/Nacc activation during the anticipation of social reward gain (i.e., approval). Stronger VS/Nacc activity during anticipation of both types of social incentives was accompanied by faster reaction times of
Acknowledgements
This work was supported by a grant from the Robert Wood Johnson Foundation (#66727) to RTS and a NINDS Postdoctoral Award (T32NS007413) to SF.
References (81)
- et al.
Parsing reward
Trends in Neurosciences
(2003) - et al.
Dissecting components of reward: “Liking”, “wanting”, and learning
Current Opinion in Pharmacology
(2009) - et al.
Dopamine in motivational control: Rewarding, aversive, and alerting
Neuron
(2010) - et al.
Biological substrates of reward and aversion: A nucleus accumbens activity hypothesis
Neuropharmacology
(2009) - et al.
The social motivation theory of autism
Trends in Cognitive Sciences
(2012) - et al.
Within- and cross-participant classifiers reveal different neural coding of information
NeuroImage
(2011) - et al.
Changes in reward-related signals in the rat nucleus accumbens measured by in vivo oxygen amperometry are consistent with fMRI BOLD responses in man
NeuroImage
(2012) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events
Neuroscience
(2000)- et al.
The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking
Brain Research Reviews
(1999) - et al.
Direct activation of the ventral striatum in anticipation of aversive stimuli
Neuron
(2003)
fMRI visualization of brain activity during a monetary incentive delay task
NeuroImage
Avoidance of harm and anxiety: A role for the nucleus accumbens
NeuroImage
From motivation to action: Functional interface between the limbic system and the motor system
Progress in Neurobiology
The nucleus accumbens as a complex of functionally distinct neuronal ensembles: An integration of behavioural, electrophysiological and anatomical data
Progress in Neurobiology
Dissociation of neural networks for anticipation and consumption of monetary and social rewards
NeuroImage
The involvement of nucleus accumbens dopamine in appetitive and aversive motivation
Behavioural Brain Research
Amygdala involvement in human avoidance, escape and approach behavior
NeuroImage
Developmental deficits in social perception in autism: The role of the amygdala and fusiform face area
International Journal of Developmental Neuroscience
ADHD related behaviors are associated with brain activation in the reward system
Neuropsychologia
Ubiquity and specificity of reinforcement signals throughout the human brain
Neuron
The genetic basis of individual differences in reward processing and the link to addictive behavior and social cognition
Neuroscience
Diagnostic and statistical manual of mental disorders, fifth edition (DSM-5)
Reward, punishment, and cooperation: A meta-analysis
Psychological Bulletin
Rewarding properties of visual stimuli
Experimental Brain Research
Development of anxiety: The role of threat appraisal and fear learning
Depression and Anxiety
Social rewards and personality
Journal of Personality and Social Psychology
Hormonal and genetic influences on processing reward and social information
Annals of the New York Academy of Sciences
Activation in the VTA and nucleus accumbens increases in anticipation of both gains and losses
Frontiers in Behavioral Neuroscience
Nucleus accumbens mediates relative motivation for rewards in the absence of choice
Frontiers in Human Neuroscience
Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies
Developmental Neuropsychology
Avoiding negative outcomes: Tracking the mechanisms of avoidance learning in humans during fear conditioning
Frontiers in Behavioral Neuroscience
Reward circuitry function in autism during face anticipation and outcomes
Journal of Autism and Developmental Disorders
Stimuli inevitably generated by behavior that avoids electric shock are inherently reinforcing
Journal of the Experimental Analysis of Behavior
An imaging genetics approach to understanding social influence
Frontiers in Human Neuroscience
Mesolimbic dopamine in desire and dread: Enabling motivation to be generated by localized glutamate disruptions in nucleus accumbens
The Journal of Neuroscience
Defining the face processing network: Optimization of the functional localizer in fMRI
Human Brain Mapping
Mechanisms of social cognition
Annual Review of Psychology
BDNF, relative preference, and reward circuitry responses to emotional communication
American Journal of Medical Genetics Part B: Neuropsychiatric Genetics
Deprivation and satiation of social reinforcers as drive conditions
The Journal of Abnormal and Social Psychology
Action dominates valence in anticipatory representations in the human striatum and dopaminergic midbrain
The Journal of Neuroscience
Cited by (111)
Impaired Punishment Learning in Conduct Disorder
2024, Journal of the American Academy of Child and Adolescent PsychiatryBalance Between Projecting Neuronal Populations of the Nucleus Accumbens Controls Social Behavior in Mice
2024, Biological PsychiatryEdge-centric functional network analyses reveal disrupted network configuration in autism spectrum disorder
2023, Journal of Affective DisordersThe neural basis of smile authenticity judgments and the potential modulatory role of the oxytocin receptor gene (OXTR)
2023, Behavioural Brain ResearchCitation Excerpt :First, the TMS technique is ideal for establishing the causal involvement of a relatively small number of brain areas [16] but is limited in identifying a broader pattern of brain activations. Furthermore, TMS cannot adequately target subcortical structures, which are known to play an essential role in smile processing [17]. Second, most neuroimaging studies on the perception of emotion authenticity have employed static images of emotional expressions [18,19] or non-visual stimuli [9,20].