Spatiotemporal dynamics across visual cortical laminae support a predictive coding framework for interpreting mismatch responses

Abstract

Abstract Context modulates neocortical processing of sensory data. Unexpected visual stimuli elicit large responses in primary visual cortex (V1)—a phenomenon known as deviance detection (DD) at the neural level, or “mismatch negativity” (MMN) when measured with EEG. It remains unclear how visual DD/MMN signals emerge across cortical layers, in temporal relation to the onset of deviant stimuli, and with respect to brain oscillations. Here we employed a visual “oddball” sequence—a classic paradigm for studying aberrant DD/MMN in neuropsychiatric populations—and recorded local field potentials in V1 of awake mice with 16-channel multielectrode arrays. Multiunit activity and current source density profiles showed that although basic adaptation to redundant stimuli was present early (50 ms) in layer 4 responses, DD emerged later (150–230 ms) in supragranular layers (L2/3). This DD signal coincided with increased delta/theta (2–7 Hz) and high-gamma (70–80 Hz) oscillations in L2/3 and decreased beta oscillations (26–36 Hz) in L1. These results clarify the neocortical dynamics elicited during an oddball paradigm at a microcircuit level. They are consistent with a predictive coding framework, which posits that predictive suppression is present in cortical feed-back circuits, which synapse in L1, whereas “prediction errors” engage cortical feed-forward processing streams, which emanate from L2/3.