Layer and rhythm specificity for predictive routing

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 117; no. 49; pp. 31459 - 31469
• Main Authors: Bastos, André M., Lundqvist, Mikael, Waite, Ayan S., Kopell, Nancy, Miller, Earl K.
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 08.12.2020
• Subjects: Action Potentials; Algorithms; Animals; Behavior, Animal; beta oscillations; Biological Sciences; Coding; cortical layers; gamma oscillations; Gamma Rhythm - physiology; Information processing; Macaca mulatta; Models, Neurological; Monkeys; Nerve Net - physiology; neural synchronization; Neurons - physiology; Neuroscience; Predictions; predictive coding; Prefrontal cortex; Psychology; psykologi; Receptive field; Spiking; Task Performance and Analysis; Time Factors; Visual stimuli; Visual tasks; cortical layers; neural synchronization; predictive coding; gamma oscillations; beta oscillations
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2014868117

In predictive coding, experience generates predictions that attenuate the feeding forward of predicted stimuli while passing forward unpredicted “errors.” Different models have suggested distinct cortical layers, and rhythms implement predictive coding. We recorded spikes and local field potentials from laminar electrodes in five cortical areas (visual area 4 [V4], lateral intraparietal [LIP], posterior parietal area 7A, frontal eye field [FEF], and prefrontal cortex [PFC]) while monkeys performed a task that modulated visual stimulus predictability. During predictable blocks, there was enhanced alpha (8 to 14 Hz) or beta (15 to 30 Hz) power in all areas during stimulus processing and prestimulus beta (15 to 30 Hz) functional connectivity in deep layers of PFC to the other areas. Unpredictable stimuli were associated with increases in spiking and in gamma-band (40 to 90 Hz) power/connectivity that fed forward up the cortical hierarchy via superficial-layer cortex. Power and spiking modulation by predictability was stimulus specific. Alpha/beta power in LIP, FEF, and PFC inhibited spiking in deep layers of V4. Area 7A uniquely showed increases in high-beta (∼22 to 28 Hz) power/connectivity to unpredictable stimuli. These results motivate a conceptual model, predictive routing. It suggests that predictive coding may be implemented via lower-frequency alpha/beta rhythms that “prepare” pathways processing-predicted inputs by inhibiting feedforward gamma rhythms and associated spiking.