Conserved features of anterior cingulate networks support observational learning across species

Burgos-Robles, Anthony; Gothard, Katalin M.; Monfils, Marie‐H.; Morozov, Alexei; Vicentic, Aleksandra

doi:10.1016/j.neubiorev.2019.09.009

Cited by 40 publications

(35 citation statements)

References 241 publications

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“…The prosocial preferences in all 3 were affected by the lesion. Despite this limitation, when taken in the context of the findings from humans, rodents, and monkeys [1,2,[4][5][6][7][8][9][11][12][13][14][17][18][19][20][21][23][24][25][26]28,29,34,43,44], our findings help further specify the role of the ACC in social cognition.…”

Section: Plos Biologymentioning

confidence: 90%

“…The body of work implicating the ACC in social processing disorders in humans [8][9][10][11][12][13][14][15]17], combined with neurophysiological and lesion studies suggesting a role for the ACC in social behavior in macaques [1,2,[23][24][25][26]28,29,34] and the current data demonstrating a causal role of the ACC in vicarious reinforcement, can help guide future research into the specific computations performed in the ACC. Moreover, several studies in rodents have demonstrated specific and causal functions of the ACC in observational fear learning [20,43], the social responses to seeing others get shocked [18,19], and the willingness to deliver a shock to a social partner [21], suggesting an evolutionarily conserved role of the ACC in mediating social learning broadly [44]. A better understanding of the causal contributions of the ACC to social information processing would come from casting a broader net to interrogate social cognition.…”

Section: Plos Biologymentioning

confidence: 99%

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The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

et al. 2020

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A key feature of most social relationships is that we like seeing good things happen to others. Research has implicated the anterior cingulate cortex (ACC) in attaching value to social outcomes. For example, single neurons in macaque ACC selectively code reward delivery to the self, a partner, both monkeys, or neither monkey. Here, we assessed whether the ACC's contribution to social cognition is causal by testing rhesus monkeys (Macaca mulatta) on a vicarious reinforcement task before and after they sustained ACC lesions. Prior to surgery, actors learned that 3 different visual cues mapped onto 3 distinct reward outcomes: to self ("Self"), to the other monkey ("Other"), or to neither monkey ("Neither"). On each trial, actors saw a cue that predicted one of the 3 juice offers and could accept the offer by making a saccade to a peripheral target or reject the offer by breaking fixation. Preoperatively, all 6 actors displayed prosocial preferences, indicated by their greater tendency to give reward to Other relative to Neither. Half then received selective, bilateral, excitotoxic lesions of the ACC, and the other half served as unoperated controls. After surgery, all monkeys retained the social preferences they had demonstrated with the preoperatively learned cues, but this preference was reduced in the monkeys with ACC lesions. Critically, none of the monkeys in the ACC lesion group acquired social preferences with a new set of cues introduced after surgery. These data indicate that the primate ACC is necessary for acquisition of prosocial preferences from vicarious reinforcement.

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Section: Plos Biologymentioning

confidence: 90%

Section: Plos Biologymentioning

confidence: 99%

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

et al. 2020

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“…Starting with the first question, of whether there are specific neural systems for social behaviour at the implementational level, the anterior cingulate cortex (ACC) is a key candidate (Figure 2). The ACC is also ideal for cross-species comparisons because it is relatively well studied in monkeys and rodents [21,38,[41][42][43][44]. Most intriguingly, evidence points to important divisions in social and non-social implementation between subregions within the ACC, particularly the sulcus (ACCs) and gyrus (ACCg) [4,21,39,42,45,46] (Figure 2).…”

Section: Opportunities and Challenges Of Cross-species Comparisonsmentioning

confidence: 99%

Is There a ‘Social’ Brain? Implementations and Algorithms

Lockwood

Apps

Chang

2020

Trends in Cognitive Sciences

163

136

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A fundamental question in psychology and neuroscience is the extent to which cognitive and neural processes are specialised for social behaviour, or are shared with other 'non-social' cognitive, perceptual, and motor faculties. Here we apply the influential framework of Marr (1982) across research in humans, monkeys, and rodents to propose that information processing can be understood as 'social' or 'non-social' at different levels. We argue that processes can be socially specialised at the implementational and/or the algorithmic level, and that changing the goal of social behaviour can also change social specificity. This framework could provide important new insights into the nature of social behaviour across species, facilitate greater integration, and inspire novel theoretical and empirical approaches. Social Specificity through the Lens of MarrMany behaviours occur in a social context. Social behaviours, in some form, are exhibited across a surprisingly broad array of species from single-celled microorganisms [1] to rodents [2], fish [3], and primates [4]. However, a core question for psychology and neuroscience is whether there are cognitive processes, brain areas, circuits, or cells that process information in a manner that is socially specific. That is, are there processes that come online only in social situations in a way that is somehow different to what is required for 'non-social' cognitive, motor, and perceptual abilities?We draw on the pioneering idea of Marr's levels (see Glossary) [5] to provide a framework to understand and test whether cognitive and neural processes are socially specialised or not. We argue that a process may be considered 'social' at the algorithmic levelit encodes a specific algorithm or rule that is different from what is being processed in a non-social domainand/or at the implementational level, the same algorithm is used, but it is processed in a different brain area, circuit, or cell. Moreover, we suggest that changing the social goal of the information-processing system (computational level), such as during cooperation or competition, can change social specialisation at the other levels. These levels of description are often overlooked when studying information processing in social contexts. We contend that this can lead to inaccurate conclusions about whether cognitive or neural processes are specialised, and call for a more nuanced approach to the phrase 'the social brain' beyond its simple connotation.

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“…The ACC is an integrative interface of sensation, cognition, emotion, arousal, and neuromodulation (Peterson et al, 1999; Bush et al, 2000; Rolls, 2019; Vassena et al, 2020), is among the most interconnected hubs in the brain (Margulies et al, 2007), and is a core region sustaining self-related processes (Northoff and Bermpohl, 2004; Qin and Northoff, 2011). The ACC contains evolutionary-conserved projections to all primary sensory and associative cortices to receive exteroceptive input; reciprocal projections to amygdala, hippocampus, ventral striatum, and VTA to enable regulation of emotion and motivation; and with OFC for processing reward and prioritizing action based on valuation (Burgos-Robles et al, 2019). Extensive reciprocal projections connect the ACC with the insula into a global paralimbic interface that combines interoceptive signals from the body with exteroceptive cues into an integrative percept that enables embodiment and emotional mirroring (Craig, 2009; Seth, 2013; Park et al, 2018), which are critical for the formation of attachment bonds.…”

Section: Discussionmentioning

confidence: 99%

Neural Representation of the Relational Self from Infancy to Adulthood

Ulmer-Yaniv¹,

Waidergoren²,

Shaked³

et al. 2021

Preprint

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Investigations into the neural underpinnings of the "self" highlight its complexity and multi-dimensionality and emphasize that various aspects of the self are sustained by different neural systems. Here, we focused on the Relational Self, a dimension denoting the self-within-attachment-relationships that taps the continuity of attachment across individual development and affiliative bonds. Mothers and children were followed across two decades and videotaped in naturalistic interactions at three ages: infancy (3-6 months), childhood (9-12 years), and young adulthood (18-24 years). During fMRI scanning, young adults were exposed to videos of their own mother-child interactions from the three ages versus matched unfamiliar interactions. Relational Self-stimuli elicited greater activations across preregistered nodes of the human caregiving network, including thalamus-to-brainstem, amygdala, hippocampus, ACC, insula, and temporal cortex. Critically, Relational Self-stimuli were age-invariant in most regions of interest despite large variability of stimuli across multiple self-related features, such as similarity, temporal distance, affect, or mentalization, and Bayesian analysis indicated strong evidence for lack of age-related differences. PPI analysis demonstrated that Relational Self-stimuli elicited tighter connectivity between the ACC and insula. Greater child social engagement during interaction with mother correlated with higher ACC and insula response to Relational Self-stimuli. Findings highlight an important novel dimension in the neural representation of the self, suggest that the Relational Self may be sustained by a paralimbic interface integrating exteroceptive and interoceptive self-related signals, and demonstrate overlap in the attachment network of parents and children, lending support to perspectives on the continuity of attachment and self across the individual's developmental history.

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Conserved features of anterior cingulate networks support observational learning across species

Cited by 40 publications

References 241 publications

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

The anterior cingulate cortex is necessary for forming prosocial preferences from vicarious reinforcement in monkeys

Is There a ‘Social’ Brain? Implementations and Algorithms

Neural Representation of the Relational Self from Infancy to Adulthood

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