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Noradrenergic alpha-2a receptor stimulation enhances prediction error signaling and updating of attention sets in anterior cingulate cortex and striatum

Author

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  • Seyed A. Hassani

    (Vanderbilt University
    Vanderbilt Brain Institute
    National Institute of Neurological Disorders and Stroke, NIH)

  • Paul Tiesinga

    (Radboud University Nijmegen)

  • Thilo Womelsdorf

    (Vanderbilt University
    Vanderbilt Brain Institute
    Vanderbilt University)

Abstract

The noradrenergic system is believed to support behavioral flexibility. A possible source mediating improved flexibility are α2A adrenoceptors (α2AR) in prefrontal cortex (PFC) or the anterior cingulate cortex (ACC). We tested this hypothesis by stimulating α2ARs using Guanfacine during attentional set shifting in male nonhuman primates. We found that α2AR stimulation improved learning from errors and updating attention sets. Neural recordings in the ACC, dorsolateral PFC, and the striatum showed that α2AR stimulation selectively enhanced neural signaling of prediction errors in neurons of the ACC and the striatum, but not in dlPFC. This modulation was accompanied by enhanced encoding of attended target features and particularly apparent in putative fast-spiking interneurons, pointing to an interneuron mediated mechanism of α2AR action. These results reveal that α2A receptors are part of the causal chain of flexibly updating attention sets through an enhancement of outcomes and prediction error signaling in ACC and striatum.

Suggested Citation

  • Seyed A. Hassani & Paul Tiesinga & Thilo Womelsdorf, 2024. "Noradrenergic alpha-2a receptor stimulation enhances prediction error signaling and updating of attention sets in anterior cingulate cortex and striatum," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-54395-8
    DOI: 10.1038/s41467-024-54395-8
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    References listed on IDEAS

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    1. Shiva Farashahi & Katherine Rowe & Zohra Aslami & Daeyeol Lee & Alireza Soltani, 2017. "Feature-based learning improves adaptability without compromising precision," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    2. Camillo Padoa-Schioppa & John A. Assad, 2006. "Neurons in the orbitofrontal cortex encode economic value," Nature, Nature, vol. 441(7090), pages 223-226, May.
    3. Mariann Oemisch & Stephanie Westendorff & Marzyeh Azimi & Seyed Alireza Hassani & Salva Ardid & Paul Tiesinga & Thilo Womelsdorf, 2019. "Feature-specific prediction errors and surprise across macaque fronto-striatal circuits," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
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