Laminar recordings in frontal cortex suggest distinct layers for maintenance and control of working memory

Significance The anatomy and dynamics of different layers of the cerebral cortex are distinct. Physiological work in the sensory cortex has investigated how different layers process sensory inputs, and how they are engaged during attention tasks. In the frontal and prefrontal cortices, where lamination is present, very few studies have investigated the role of distinct layers for cognition. We studied frontal cortex laminar neuronal activity as monkeys performed working memory tasks. Spiking and gamma-band activity (50–150 Hz) in the superficial layers reflected active maintenance of working memories. Alpha/beta frequencies (4–22 Hz) in the deep layers modulated the gamma activity in the superficial layers. This might serve a control function, allowing information to enter or exit active storage in superficial layers. All of the cerebral cortex has some degree of laminar organization. These different layers are composed of neurons with distinct connectivity patterns, embryonic origins, and molecular profiles. There are little data on the laminar specificity of cognitive functions in the frontal cortex, however. We recorded neuronal spiking/local field potentials (LFPs) using laminar probes in the frontal cortex (PMd, 8A, 8B, SMA/ACC, DLPFC, and VLPFC) of monkeys performing working memory (WM) tasks. LFP power in the gamma band (50–250 Hz) was strongest in superficial layers, and LFP power in the alpha/beta band (4–22 Hz) was strongest in deep layers. Memory delay activity, including spiking and stimulus-specific gamma bursting, was predominately in superficial layers. LFPs from superficial and deep layers were synchronized in the alpha/beta bands. This was primarily unidirectional, with alpha/beta bands in deep layers driving superficial layer activity. The phase of deep layer alpha/beta modulated superficial gamma bursting associated with WM encoding. Thus, alpha/beta rhythms in deep layers may regulate the superficial layer gamma bands and hence maintenance of the contents of WM.