Cortical networks with multiple interneuron types generate oscillatory patterns during predictive coding

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Abstract

Predictive coding (PC) proposes that our brains work as an inference machine, generating an internal model of the world and minimizing predictions errors (i.e., differences between external sensory evidence and internal prediction signals). Theoretical models of PC often rely on high-level approaches, and therefore implementations detailing which neurons or pathways are used to compute prediction errors or adapt the internal representations, as well as their level of agreement with biological circuitry, are currently missing. Here we propose a computational model of PC, which integrates a neuroanatomically informed hierarchy of cortical areas with a precise laminar organization and cell-type-specific connectivity between pyramidal, PV, SST and VIP cells. Our model efficiently performs PC, even in the presence of external and internal noise, by forming latent representations of naturalistic visual input (MNIST, fashion-MNIST and grayscale CIFAR-10) via Hebbian learning and using them to predict sensory input by minimizing prediction errors. The model assumes that both positive and negative prediction errors are computed by stereotypical pyramidal-PV-SST-VIP circuits with the same structure but different incoming input. During sensory inference, neural oscillatory activity emerges in the system due to interactions between representation and prediction error microcircuits, with optogenetics-inspired inactivation protocols revealing a differentiated role of PV, SST and VIP cell types in such dynamics. Finally, our model shows anomalous responses to deviant stimuli within series of same-image presentations, in agreement with experimental results on mismatch negativity and oddball paradigms. We argue that our model constitutes an important step to better understand the circuits mediating PC in real cortical networks.

Author summary

Predictive coding (PC) suggests that the brain constantly generates expectations about the world and updates these expectations based on incoming sensory input. While this theory is widely accepted, we still lack detailed models that show how specific neurons and brain circuits might carry out these processes. Here, we present a computational model which addresses this gap by including biologically plausible brain circuitry with specific types of neurons (pyramidal, PV, SST, and VIP cells) and their connections. It efficiently learns to form internal representations of visual information and uses them to predict sensory input, adjusting its predictions when errors occur. We found that particular types of neurons play different roles in these processes, and that neural oscillations emerge during the training and inference processes. Our model also replicates neural patterns observed in experiments where unexpected stimuli appear. By integrating anatomical and functional details, our work brings us closer to understanding how the brain uses predictive coding at the circuit level.

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