Primate Amygdala Neurons Simulate Decision Processes of Social Partners

Grabenhorst, Fabian; Báez-Mendoza, Raymundo; Genest, Wilfried; Deco, Gustavo; Schultz, Wolfram

doi:10.1016/j.cell.2019.02.042

Cited by 82 publications

(101 citation statements)

References 57 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Neither the fine grain single unit literature nor the coarser neuroimaging literature brought conclusive evidence for or against the functional compartmentalization of the primate amygdala. Only a small fraction of the single unit studies reported an uneven distribution of neurons with particular response properties across the nuclei (e.g., Clayton P Mosher, Zimmerman, and Gothard 2010; Zhang et al 2013;Grabenhorst et al 2019). To complicate things further, an increasing number of single unit studies reported that neurons in the amygdala respond to multiple stimulus dimensions and task parameters (Saez et al 2015;Kyriazi, Headley, and Pare 2018b;Munuera, Rigotti, and Salzman 2018;Morrow, Mosher, and Gothard 2019;Putnam and Gothard 2019).…”

Section: Resultsmentioning

confidence: 99%

Mesoscopic-scale functional networks in the primate amygdala

Morrow

Cohen

Gothard

2020

Preprint

View full text Add to dashboard Cite

The primate amygdala performs multiple functions that may be related to the anatomical heterogeneity of its nuclei. At the level of single neurons, each function is reflected in stimulus-and taskspecific responses. Given that neurons with a particular response profile are not clustered in any of the nuclei, single units may be too fine-grained to shed light on the mesoscale organization of the amygdala.We have extracted from local field potentials recorded simultaneously from multiple locations within the primate amygdala (Macaca mulatta) spatially defined and statistically separable responses to visual, tactile, and auditory stimuli. A generalized eigendecomposition-based method of source separation isolated coactivity patterns, or components, that in neurophysiological terms correspond to putative subnetworks. Some component spatial patterns mapped onto the anatomical organization of the amygdala, while other components reflected integration across nuclei. These components differentiated between visual, tactile, and auditory stimuli suggesting the presence of functionally distinct parallel subnetworks.

show abstract

Section: Resultsmentioning

confidence: 99%

Mesoscopic-scale functional networks in the primate amygdala

Morrow

Cohen

Gothard

2020

Preprint

View full text Add to dashboard Cite

show abstract

“…These neurons have previously been shown to have properties resembling ‘mirror’ neurons 34-37 , but their role in the cultural transmission of vocal behaviors was not well understood. The functional significance of mirror neurons in behavioral imitation and ASD is a topic of much debate 38-43 . We show that knockdown of FoxP1 in striatal projecting HVC X neurons clamps their spine plasticity, dampens their intrinsic excitability, and blocks the cellular and network level signatures associated with tutor-song memory formation following social experience.…”

Section: Discussionmentioning

confidence: 99%

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

García-Oscos

Koch

Pancholi

et al. 2020

Preprint

View full text Add to dashboard Cite

Autism spectrum disorders (ASD) are characterized by impaired learning of culturally transmitted behaviors like 10 social skills, speech, and language 1-3 . These behaviors are learned by copying parents and other social models during 11 development, a two-stage process that involves forming memories of appropriate behaviors during social 12 experiences and then using those memories to guide imitation. How ASD-linked genes impair these often-13 intertwined aspects of learning is not known, thereby limiting our understanding of the developmental progression 14 of ASD and the targeting of therapeutic interventions. Here we show that these aspects of learning are dissociable 15 and that the ASD-linked gene FoxP1 selectively impairs learning from social experience, but not behavioral imitation. 16 Haploinsufficiency of FOXP1 in humans causes FOXP1 syndrome, a neurodevelopmental disorder typified by severe 17 disruptions in speech and language development, and other ASD-associated symptoms 4,5 . We tested how 18 knockdown of FoxP1 (FP1-KD) affects the cultural transmission of vocal behaviors in zebra finches, a songbird that 19 learns by memorizing and vocally copying the song of an adult 'song-tutor'. We find that FP1-KD blocks song learning20 in juvenile birds by selectively impairing their ability to encode a memory during social experiences with a song-21 tutor. These learning deficits are linked to disruptions in experience-driven structural and functional plasticity. 22However, if birds are exposed to tutor-song prior to FP1-KD, their ability to imitate that song during development is 23 unaffected. Thus, FP1-KD impairs cultural transmission of vocalizations by disrupting the ability to form appropriate 24 vocal memories, yet spares the ability to use previously acquired memories to guide vocal learning. This indicates 25 that learning from social experience may be particularly vulnerable in FOXP1 syndrome. 26 27 28Humans and other animals learn many of their complex and socially oriented behaviors by imitating more experienced 29 individuals in their environment. For example, development of spoken language is rooted in a child's ability to imitate 30 the speech patterns of their parent(s) and other adults 6-8 . This cultural transmission of behavior is impaired in many 31 neurodevelopmental disorders, most notably ASD 1-3 . However, how ASD risk genes impact behavioral imitation is still 32 not known. We sought to examine this issue by testing the role of FoxP1 in the cultural transmission of song between 33 adult and juvenile zebra finches ( Fig. 1a-d, Extended Data Fig. 1). 34 35 2 FOXP1 (forkhead-box protein 1) is one of the top ASD-associated genes, and its haploinsufficiency causes specific 36 language impairment and intellectual disability in children 5 . FoxP1 is expressed in many of the same areas of the pallium 37 and basal ganglia in mammals and songbirds 9-11 . In zebra finches, FoxP1 expression is enriched in many brain regions 38 that are known to be important for song learning [10][11][12] (Fig. ...

show abstract

“…This limits our ability to guess what information might be passing between the frontal and temporal regions. Yet, there is an increasing number of studies examining social behaviour between more than one subject (Grabenhorst, Báez-Mendoza, Genest, Deco, & Schultz, 2019;Haroush & Williams, 2015;K. Yoshida et al, 2012), so it is becoming more feasible to conduct experiments involving two or more monkeys interacting with one another.…”

Section: Future Directionsmentioning

confidence: 99%

Perceived ambiguity of social interactions increases coupling between frontal and temporal nodes of the social brain

Ainsworth

Sallet

Joly

et al. 2020

Preprint

View full text Add to dashboard Cite

Social behaviour is coordinated by a network of brain regions, including those involved in the perception of social stimuli and those involved in complex functions like inferring perceptual and mental states and controlling social interactions. The properties and function of many of these regions in isolation is relatively well understood but little is known about how these regions interact whilst processing dynamic social interactions. To investigate whether social network connectivity is modulated by social context we collected fMRI data from monkeys viewing "affiliative", "aggressive", or "ambiguous" social interactions. We show activation relating to the perception of social interactions along both banks of the superior temporal sulcus, parietal, medial and lateral PFC and caudate nucleus. Within this network we demonstrate that fronto-temporal connectivity are significantly modulated by social context. Crucially, we link the observation of specific behaviours to changes in connectivity within our network. Viewing aggressive or affiliative behaviour was associated with a limited increase in temporo-temporal and premotor-temporal connectivity respectively. By contrast, viewing ambiguous interactions was associated with a pronounced increase in cingulatecingulate, temporo-temporal, and cingulate-temporal connectivity. We hypothesise that this widespread network synchronisation occurs when cingulate and temporal areas coordinate their activity when more difficult social inferences are made.

show abstract

Primate Amygdala Neurons Simulate Decision Processes of Social Partners

Cited by 82 publications

References 57 publications

Mesoscopic-scale functional networks in the primate amygdala

Mesoscopic-scale functional networks in the primate amygdala

Autism-linked gene FoxP1 selectively regulates the cultural transmission of learned vocalizations

Perceived ambiguity of social interactions increases coupling between frontal and temporal nodes of the social brain

Contact Info

Product

Resources

About