Adolescent frontal top-down neurons receive heightened local drive to establish adult attentional behavior in mice

• Published in: Nature communications Vol. 11; no. 1; p. 3983
• Main Authors: Nabel, Elisa M, Garkun, Yury, Koike, Hiroyuki, Sadahiro, Masato, Liang, Ana, Norman, Kevin J, Taccheri, Giulia, Demars, Michael P, Im, Susanna, Caro, Keaven, Lopez, Sarah, Bateh, Julia, Hof, Patrick R, Clem, Roger L, Morishita, Hirofumi
• Format: Journal Article
• Language: English
• Published: England Nature Publishing Group 07.08.2020; Nature Publishing Group UK; Nature Portfolio
• Subjects: Action Potentials - physiology; Adolescents; Aging - physiology; Animals; Attention - physiology; Behavior, Animal - physiology; Channelrhodopsins - metabolism; Child development; Circuits; Cortex (frontal); Critical period; Gyrus Cinguli - physiology; Male; Mapping; Mice; Mice, Inbred C57BL; Models, Neurological; Neural Inhibition - physiology; Neural networks; Neurons; Neurons - physiology; Presynaptic Terminals - physiology; Rabies; Rabies - physiopathology; Sensory neurons; Somatosensory cortex; Synapses - physiology; Vision, Ocular - physiology; Visual cortex; Visual pathways
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-020-17787-0

Frontal top-down cortical neurons projecting to sensory cortical regions are well-positioned to integrate long-range inputs with local circuitry in frontal cortex to implement top-down attentional control of sensory regions. How adolescence contributes to the maturation of top-down neurons and associated local/long-range input balance, and the establishment of attentional control is poorly understood. Here we combine projection-specific electrophysiological and rabies-mediated input mapping in mice to uncover adolescence as a developmental stage when frontal top-down neurons projecting from the anterior cingulate to visual cortex are highly functionally integrated into local excitatory circuitry and have heightened activity compared to adulthood. Chemogenetic suppression of top-down neuron activity selectively during adolescence, but not later periods, produces long-lasting visual attentional behavior deficits, and results in excessive loss of local excitatory inputs in adulthood. Our study reveals an adolescent sensitive period when top-down neurons integrate local circuits with long-range connectivity to produce attentional behavior.