Multimodal mechanisms of human socially reinforced learning across neurodegenerative diseases

Brain : a journal of neurology

Brain. 2021 Sep 16:awab345. doi: 10.1093/brain/awab345. Online ahead of print.

ABSTRACT

Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioral variant frontotemporal dementia (n = 21), Parkinson's disease (n = 31), and Alzheimer's disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning, and associative learning respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioral task with ongoing electroencephalographic (EEG) signatures of implicit learning (medial frontal negativity) and offline magnetic resonance imaging (MRI) measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioral variant frontotemporal dementia and Parkinson's disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer's disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioral variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioral variant frontotemporal dementia, and predominantly fronto-limbic regions in Alzheimer's disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson's disease. Results are consistent with core social deficits in behavioral variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson's disease, and generalized learning alterations in Alzheimer's disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially-reinforced learning and neurodegeneration.

PMID:34529034 | DOI:10.1093/brain/awab345

Authors

Agustina Legaz
Sofía Abrevaya
Martín Dottori
Cecilia González Campo
Agustina Birba
Miguel Martorell Caro
Julieta Aguirre
Andrea Slachevsky
Rafael Aranguiz
Cecilia Serrano
Claire M Gillan
Iracema Leroi
Adolfo M García
Sol Fittipaldi
Agustín Ibañez