Linking Brain Structure and Activation in Temporoparietal Junction to Explain the Neurobiology of Human Altruism

Morishima, Yosuke; Schunk, Daniel; Bruhin, Adrian; Ruff, Christian C.; Fehr, Ernst

doi:10.1016/j.neuron.2012.05.021

Cited by 254 publications

(271 citation statements)

References 35 publications

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“…1). In the human temporoparietal cortex, the voxels most likely to have the template connectivity profile were located at the posterior end of the superior temporal sulcus, at the location previously attributed to the part of the TPJ area associated with ToM and social preference (8,9,22) (Fig. 2, Upper Right).…”

Section: Resultsmentioning

confidence: 80%

“…It has been argued that this ability is uniquely human (6) and forms the basis of our distinctive ability to cooperate, leading to culture and ultimately language (7). TPJ is also associated with "social preferences" and the predisposition to take into account the benefit that might accrue to others as well as to oneself when making a decision (8,9). Such predispositions are present in monkeys but their neural basis is only beginning to be elucidated (10,11).…”

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confidence: 99%

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Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

Mars

Sallet

Neubert

et al. 2013

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

154

165

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The human ability to infer the thoughts and beliefs of others, often referred to as "theory of mind," as well as the predisposition to even consider others, are associated with activity in the temporoparietal junction (TPJ) area. Unlike the case of most human brain areas, we have little sense of whether or how TPJ is related to brain areas in other nonhuman primates. It is not possible to address this question by looking for similar task-related activations in nonhuman primates because there is no evidence that nonhuman primates engage in theory-of-mind tasks in the same manner as humans. Here, instead, we explore the relationship by searching for areas in the macaque brain that interact with other macaque brain regions in the same manner as human TPJ interacts with other human brain regions. In other words, we look for brain regions with similar positions within a distributed neural circuit in the two species. We exploited the fact that human TPJ has a unique functional connectivity profile with cortical areas with known homologs in the macaque. For each voxel in the macaque temporal and parietal cortex we evaluated the similarity of its functional connectivity profile to that of human TPJ. We found that areas in the middle part of the superior temporal cortex, often associated with the processing of faces and other social stimuli, have the most similar connectivity profile. These results suggest that macaque face processing areas and human mentalizing areas might have a similar precursor.comparative anatomy | cooperation | comparative cognition F or a social species like our own, evolutionary success necessitates the ability to navigate a world full of conspecifics. Consequently, humans are extremely sensitive to information about others' emotional states or intentions as provided by cues such as facial expression or body movement. Supporting these abilities, the human temporal cortex contains a number of areas involved in the processing of such social information (1-5). An area that has received particular emphasis in the study of human social abilities is located at the posterior end of the superior temporal sulcus (STS), at the junction with the parietal cortex. This temporoparietal junction (TPJ) area has been implicated in the human ability to attribute belief states to others, so-called "mentalizing" or "theory of mind" (ToM). It has been argued that this ability is uniquely human (6) and forms the basis of our distinctive ability to cooperate, leading to culture and ultimately language (7). TPJ is also associated with "social preferences" and the predisposition to take into account the benefit that might accrue to others as well as to oneself when making a decision (8, 9). Such predispositions are present in monkeys but their neural basis is only beginning to be elucidated (10, 11).In trying to establish the evolutionary origin of human social abilities, research into the processing of social information in the macaque temporal cortex has demonstrated the existence of a number of areas responsive to fac...

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Section: Resultsmentioning

confidence: 80%

mentioning

confidence: 99%

Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

Mars

Sallet

Neubert

et al. 2013

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

154

165

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“…Therefore, if this hypothesis is true, TPJ activation should correlate positively with the social-distance-dependent ORU. This view of the role of the TPJ is challenged by more recent studies postulating that TPJ activation solves the conflict between generous and selfish motives (16). According to this hypothesis, to make a generous decision, the putatively natural bias to maximize own-payoff needs to be overcome (18).…”

Section: Significancementioning

confidence: 99%

“…To this end, we tested the predictions of two competing ideas on the role of the TPJ during prosocial choice in general, and social discounting in particular. Previous research showed that this region is involved in tasks requiring the ability to represent and understand others' perspectives (12,13) and in social and selfish decisions (14)(15)(16)(17). Thus, the TPJ's implication in prosocial choice, perspective taking, empathizing, and ToM suggests that it plays a role in…”

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confidence: 99%

Social discounting involves modulation of neural value signals by temporoparietal junction

Strombach

Weber

Hangebrauk

et al. 2015

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

183

230

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Most people are generous, but not toward everyone alike: generosity usually declines with social distance between individuals, a phenomenon called social discounting. Despite the pervasiveness of social discounting, social distance between actors has been surprisingly neglected in economic theory and neuroscientific research. We used functional magnetic resonance imaging (fMRI) to study the neural basis of this process to understand the neural underpinnings of social decision making. Participants chose between selfish and generous alternatives, yielding either a large reward for the participant alone, or smaller rewards for the participant and another individual at a particular social distance. We found that generous choices engaged the temporoparietal junction (TPJ). In particular, the TPJ activity was scaled to the social-distance-dependent conflict between selfish and generous motives during prosocial choice, consistent with ideas that the TPJ promotes generosity by facilitating overcoming egoism bias. Based on functional coupling data, we propose and provide evidence for a biologically plausible neural model according to which the TPJ supports social discounting by modulating basic neural value signals in the ventromedial prefrontal cortex to incorporate social-distancedependent other-regarding preferences into an otherwise exclusively own-reward value representation.social discounting | prosocial choice | fMRI | connectivity | neuroeconomics P rosociality is one of the most fundamental qualities of all human societies. Without the ability to take other people's interests into account, human relationships would disintegrate and societies would malfunction. It has been widely demonstrated in laboratory and field experiments that individuals consider the welfare of others in their decisions and the consequences a decision has on them (1-3). Although almost all of us behave prosocially at times, it is clear that people are not equally generous to everyone alike. Rather, generosity decreases as a function of the closeness of the relationship between two individuals (2, 4). However, it is currently unknown how social distance contributes to the decision process on a neural level. In the present study, we set out to address this question.Our first aim was to investigate the systematic influence of social-distance-dependent levels of generosity on neural activation. This was investigated using a social discounting experiment adapted to the functional magnetic resonance imaging (fMRI) environment (1). We measured blood oxygen leveldependent (BOLD) responses while subjects made choices between selfish and generous rewards for themselves and for other people that varied in social distance. Choosing selfishly yielded a payoff only for the subject, whereas making a generous choice resulted in a lower payoff for the subject coupled with a reward for another person at a specific social distance (Fig. 1). Next, based on the individual choices, we reconstructed the socialdistance-dependent other-regarding utility (ORU), tha...

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“…We implemented a modified version of the dictator game, based on the design by Morishima and colleagues,21 so that we relied upon the distribution of the monetary splits verbally rather than visually. Participants were required to state how they would like to readjust the presented monetary spilt (e.g., you have £7 and the stranger has £3).…”

Section: Methodsmentioning

confidence: 99%

Biased numerical cognition impairs economic decision‐making in Parkinson's disease

Arshad

Bonsu

Lobo

et al. 2017

Ann Clin Transl Neurol

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ObjectivePrevious findings suggest a context‐dependent bihemispheric allocation of numerical magnitude. Accordingly, we predicted that lateralized motor symptoms in Parkinson's disease (PD), which reflect hemispheric asymmetries, would induce systematic lateralized biases in numerical cognition and have a subsequent influence on decision‐making.MethodsIn 20 PD patients and matched healthy controls we assessed numerical cognition using a number‐pair bisection and random number generation task. Decision‐making was assessed using both the dictator game and a validated questionnaire.Results PD patients with predominant right‐sided motor symptoms exhibited pathological biases toward smaller numerical magnitudes and formulated less favorable prosocial choices during a neuroeconomics task (i.e., dictator game). Conversely, patients with left‐sided motor symptoms exhibited pathological biases toward larger numerical magnitudes and formulated more generous prosocial choices. Our account of context‐dependent hemispheric allocation of numerical magnitude in PD was corroborated by applying our data to a pre‐existing computational model and observing significant concordance. Notably, both numerical biasing and impaired decision‐making were correlated with motor asymmetry.InterpretationAccordingly, motor asymmetry and functional impairment of cognitive processes in PD can be functionally intertwined. To conclude, our findings demonstrate context‐dependent hemispheric allocation and encoding of numerical magnitude in PD and how biases in numerical magnitude allocation in Parkinsonian patients can correspondingly impair economic decision‐making.

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Linking Brain Structure and Activation in Temporoparietal Junction to Explain the Neurobiology of Human Altruism

Cited by 254 publications

References 35 publications

Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

Connectivity profiles reveal the relationship between brain areas for social cognition in human and monkey temporoparietal cortex

Social discounting involves modulation of neural value signals by temporoparietal junction

Biased numerical cognition impairs economic decision‐making in Parkinson's disease

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