Amygdaloid projections to ventromedial striatal subterritories in the primate

Fudge, Julie L.; Kunishio, Katsuzo; Walsh, Peter; Richard, Christian; Haber, Suzanne N.

doi:10.1016/s0306-4522(01)00546-2

Cited by 204 publications

(171 citation statements)

References 86 publications

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“…BLA has elaborate and reciprocal connections with prefrontal cortex (58) and projects to the nucleus accumbens in the ventral striatum (59,60), endorsing a role for the amygdala in shaping how these circuits process the value of rewards during decisionmaking. We speculate that mirroring of reward values for self and others by BLA serves to adjust the gain of neuronal signals mediating social decisions in the brain.…”

Section: Discussionmentioning

confidence: 99%

Neural mechanisms of social decision-making in the primate amygdala

Chang

Fagan

Toda

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

134

117

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Social decisions require evaluation of costs and benefits to oneself and others. Long associated with emotion and vigilance, the amygdala has recently been implicated in both decision-making and social behavior. The amygdala signals reward and punishment, as well as facial expressions and the gaze of others. Amygdala damage impairs social interactions, and the social neuropeptide oxytocin (OT) influences human social decisions, in part, by altering amygdala function. Here we show in monkeys playing a modified dictator game, in which one individual can donate or withhold rewards from another, that basolateral amygdala (BLA) neurons signaled social preferences both across trials and across days. BLA neurons mirrored the value of rewards delivered to self and others when monkeys were free to choose but not when the computer made choices for them. We also found that focal infusion of OT unilaterally into BLA weakly but significantly increased both the frequency of prosocial decisions and attention to recipients for context-specific prosocial decisions, endorsing the hypothesis that OT regulates social behavior, in part, via amygdala neuromodulation. Our findings demonstrate both neurophysiological and neuroendocrinological connections between primate amygdala and social decisions.amygdala | social decision | value mirroring | oxytocin | hierarchical modeling H ow we treat others impacts not only their well-being but our own. Human society depends on cooperation, charity, and altruism, as well as institutions to regulate selfish biases. In humans, these behaviors involve perspective-taking, empathy, and theory of mind (1, 2), and the rudiments of these capacities appear to mediate complex social behavior in animals (3). Recent research has sketched a rough outline of the neural circuits that contribute to complex social behavior (4, 5). These comprise a set of domaingeneral brain areas, including the ventromedial prefrontal cortex and ventral striatum, that process information about reward and punishment and contribute to decision-making, and a set of specialized areas, including the temporoparietal junction and medial prefrontal cortex, that process specifically social information (4, 6). How social and nonsocial signals in these circuits are integrated to mediate decisions with respect to others remains imperfectly understood, in part, due to the indirect nature of hemodynamic signals measured in human neuroimaging experiments that constitute the bulk of this research. Recent advances in the development of neurophysiological and neuropharmacological models of social decision-making, however, permit more direct inquiry into the neural mechanisms mediating other-regarding behavior (7-11).The amygdala, especially the basolateral division (BLA), has been implicated in both decision-making and social perception, inviting the possibility that it contributes to decision-making with respect to others (12)(13)(14)(15)(16)(17). This set of nuclei is well known for contributions to emotional experience and expression, especia...

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Section: Discussionmentioning

confidence: 99%

Neural mechanisms of social decision-making in the primate amygdala

Chang

Fagan

Toda

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

134

117

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“…However, striatal neurons receive afferents from many cortical and subcortical structures involved in social processes (18,32), which could give rise to the observed activities. As striatal neurons link own action with own reward (33), converging inputs and local interactions in the striatum (34) are also well suited to combine information about other's actions and own reward.…”

Section: Discussionmentioning

confidence: 99%

Activity of striatal neurons reflects social action and own reward

Báez-Mendoza

Harris

Schultz

2013

Proc. Natl. Acad. Sci. U.S.A.

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Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific's reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.

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“…The VS also contains many pallidal cells and their dendritic arbors that invade this ventral forebrain territory (see section Ventral pallidum). Finally, and of particular importance, is the fact that while both the dorsal and VS receive input from the cortex, thalamus, and brainstem, the VS alone receives a dense projection from the amygdala and hippocampus (Friedman et al, 2002;Fudge et al, 2002;Russchen et al, 1985). (Figure 3).…”

Section: Organization Of the Vsmentioning

confidence: 99%

“…Overall, the basal nucleus and the magnocellular division of the accessory basal nucleus are the main source of inputs to the VS (Fudge et al, 2002;Russchen et al, 1985). The lateral nucleus has a relatively minor input to the VS.…”

Section: Connections Of the Vsmentioning

confidence: 99%

The Reward Circuit: Linking Primate Anatomy and Human Imaging

Haber

Knutson

2009

Neuropsychopharmacol

3,175

193

2,859

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Although cells in many brain regions respond to reward, the cortical-basal ganglia circuit is at the heart of the reward system. The key structures in this network are the anterior cingulate cortex, the orbital prefrontal cortex, the ventral striatum, the ventral pallidum, and the midbrain dopamine neurons. In addition, other structures, including the dorsal prefrontal cortex, amygdala, hippocampus, thalamus, and lateral habenular nucleus, and specific brainstem structures such as the pedunculopontine nucleus, and the raphe nucleus, are key components in regulating the reward circuit. Connectivity between these areas forms a complex neural network that mediates different aspects of reward processing. Advances in neuroimaging techniques allow better spatial and temporal resolution. These studies now demonstrate that human functional and structural imaging results map increasingly close to primate anatomy.

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Amygdaloid projections to ventromedial striatal subterritories in the primate

Cited by 204 publications

References 86 publications

Neural mechanisms of social decision-making in the primate amygdala

Neural mechanisms of social decision-making in the primate amygdala

Activity of striatal neurons reflects social action and own reward

The Reward Circuit: Linking Primate Anatomy and Human Imaging

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