Laminar pattern of adolescent development changes in working memory neuronal activity

• Published in: Journal of neurophysiology 2023-10, Vol.130 (4), p.980-989
• Main Authors: Zhu, Junda, Hammond, Benjamin M, Zhou, Xin Maizie, Constantinidis, Christos
• Format: Article
• Language: English
• Subjects: Adolescent Development; Animals; Cognition - physiology; Humans; Male; Memory, Short-Term - physiology; Neurons - physiology; Prefrontal Cortex - physiology
• ISSN: 0022-3077; 1522-1598; 1522-1598
• DOI: 10.1152/jn.00294.2023

Adolescent development is characterized by an improvement in cognitive abilities, such as working memory. Neurophysiological recordings in a nonhuman primate model of adolescence have revealed changes in neural activity that mirror improvement in behavior, including higher firing rate during the delay intervals of working memory tasks. The laminar distribution of these changes is unknown. By some accounts, persistent activity is more pronounced in superficial layers, so we sought to determine whether changes are most pronounced there. We therefore analyzed neurophysiological recordings from the young and adult stage of male monkeys, at different cortical depths. Superficial layers exhibited an increased baseline firing rate in the adult stage. Unexpectedly, we also detected substantial increases in delay period activity in the middle layers after adolescence, which was confirmed even after excluding penetrations near sulci. Finally, improved discriminability around the saccade period was most evident in the deeper layers. These results reveal the laminar pattern of neural activity maturation that is associated with cognitive improvement. Structural brain changes are evident during adolescent development particularly in the cortical thickness of the prefrontal cortex, at a time when working memory ability increases markedly. The depth distribution of neurophysiological changes during adolescence is not known. Here, we show that neurophysiological changes are not confined to superficial layers, which have most often been implicated in the maintenance of working memory. Contrary to expectations, substantial changes were evident in intermediate layers of the prefrontal cortex.