Large-scale interactions in predictive processing: oscillatory versus transient dynamics.

How do the two main types of neural dynamics, aperiodic transients and oscillations, contribute to the interactions between feedforward (FF) and feedback (FB) pathways in sensory inference and predictive processing? We discuss three theoretical perspectives. First, we critically evaluate the theory that gamma and alpha/beta rhythms play a role in classic hierarchical predictive coding (HPC) by mediating FF and FB communication, respectively. Second, we outline an alternative functional model in which rapid sensory inference is mediated by aperiodic transients, whereas oscillations contribute to the stabilization of neural representations over time and plasticity processes. Third, we propose that the strong dependence of oscillations on predictability can be explained based on a biologically plausible alternative to classic HPC, namely dendritic HPC.

Distributed representations of prediction error signals across the cortical hierarchy are synergistic.

A relevant question concerning inter-areal communication in the cortex is whether these interactions are synergistic. Synergy refers to the complementary effect of multiple brain signals conveying more information than the sum of each isolated signal. Redundancy, on the other hand, refers to the common information shared between brain signals. Here, we dissociated cortical interactions encoding complementary information (synergy) from those sharing common information (redundancy) during prediction error (PE) processing. We analyzed auditory and frontal electrocorticography (ECoG) signals in five common awake marmosets performing two distinct auditory oddball tasks and investigated to what extent event-related potentials (ERP) and broadband (BB) dynamics encoded synergistic and redundant information about PE processing. The information conveyed by ERPs and BB signals was synergistic even at lower stages of the hierarchy in the auditory cortex and between auditory and frontal regions. Using a brain-constrained neural network, we simulated the synergy and redundancy observed in the experimental results and demonstrated that the emergence of synergy between auditory and frontal regions requires the presence of strong, long-distance, feedback, and feedforward connections. These results indicate that distributed representations of PE signals across the cortical hierarchy can be highly synergistic.

Self-Relevance Predicts the Aesthetic Appeal of Real and Synthetic Artworks Generated via Neural Style Transfer.

What determines the aesthetic appeal of artworks? Recent work suggests that aesthetic appeal can, to some extent, be predicted from a visual artwork's image features. Yet a large fraction of variance in aesthetic ratings remains unexplained and may relate to individual preferences. We hypothesized that an artwork's aesthetic appeal depends strongly on self-relevance. In a first study (N = 33 adults, online replication N = 208), rated aesthetic appeal for real artworks was positively predicted by rated self-relevance. In a second experiment (N = 45 online), we created synthetic, self-relevant artworks using deep neural networks that transferred the style of existing artworks to photographs. Style transfer was applied to self-relevant photographs selected to reflect participant-specific attributes such as autobiographical memories. Self-relevant, synthetic artworks were rated as more aesthetically appealing than matched control images, at a level similar to human-made artworks. Thus, self-relevance is a key determinant of aesthetic appeal, independent of artistic skill and image features.

Cell-type-specific propagation of visual flicker.

Rhythmic flicker stimulation has gained interest as a treatment for neurodegenerative diseases and as a method for frequency tagging neural activity. Yet, little is known about the way in which flicker-induced synchronization propagates across cortical levels and impacts different cell types. Here, we use Neuropixels to record from the lateral geniculate nucleus (LGN), the primary visual cortex (V1), and CA1 in mice while presenting visual flicker stimuli. LGN neurons show strong phase locking up to 40 Hz, whereas phase locking is substantially weaker in V1 and is absent in CA1. Laminar analyses reveal an attenuation of phase locking at 40 Hz for each processing stage. Gamma-rhythmic flicker predominantly entrains fast-spiking interneurons. Optotagging experiments show that these neurons correspond to either parvalbumin (PV+) or narrow-waveform somatostatin (Sst+) neurons. A computational model can explain the observed differences based on the neurons' capacitative low-pass filtering properties. In summary, the propagation of synchronized activity and its effect on distinct cell types strongly depend on its frequency.

Principles of large-scale neural interactions.

What mechanisms underlie flexible inter-areal communication in the cortex? We consider four mechanisms for temporal coordination and their contributions to communication: (1) Oscillatory synchronization (communication-through-coherence); (2) communication-through-resonance; (3) non-linear integration; and (4) linear signal transmission (coherence-through-communication). We discuss major challenges for communication-through-coherence based on layer- and cell-type-specific analyses of spike phase-locking, heterogeneity of dynamics across networks and states, and computational models for selective communication. We argue that resonance and non-linear integration are viable alternative mechanisms that facilitate computation and selective communication in recurrent networks. Finally, we consider communication in relation to cortical hierarchy and critically examine the hypothesis that feedforward and feedback communication use fast (gamma) and slow (alpha/beta) frequencies, respectively. Instead, we propose that feedforward propagation of prediction errors relies on the non-linear amplification of aperiodic transients, whereas gamma and beta rhythms represent rhythmic equilibrium states that facilitate sustained and efficient information encoding and amplification of short-range feedback via resonance.

Predictive coding of natural images by V1 firing rates and rhythmic synchronization.

Predictive coding is an important candidate theory of self-supervised learning in the brain. Its central idea is that sensory responses result from comparisons between bottom-up inputs and contextual predictions, a process in which rates and synchronization may play distinct roles. We recorded from awake macaque V1 and developed a technique to quantify stimulus predictability for natural images based on self-supervised, generative neural networks. We find that neuronal firing rates were mainly modulated by the contextual predictability of higher-order image features, which correlated strongly with human perceptual similarity judgments. By contrast, V1 gamma (γ)-synchronization increased monotonically with the contextual predictability of low-level image features and emerged exclusively for larger stimuli. Consequently, γ-synchronization was induced by natural images that are highly compressible and low-dimensional. Natural stimuli with low predictability induced prominent, late-onset beta (ß)-synchronization, likely reflecting cortical feedback. Our findings reveal distinct roles of synchronization and firing rates in the predictive coding of natural images.

A mechanism for inter-areal coherence through communication based on connectivity and oscillatory power.

Inter-areal coherence between field potentials is a widespread phenomenon in cortex. Coherence has been hypothesized to reflect phase-synchronization between oscillators and flexibly gate communication according to behavioral and cognitive demands. We reveal an alternative mechanism where coherence is not the cause but the consequence of communication and naturally emerges because spiking activity in a sending area causes post-synaptic potentials both in the same and in other areas. Consequently, coherence depends in a lawful manner on power and phase-locking in the sender and connectivity. Changes in oscillatory power explained prominent changes in fronto-parietal and LGN-V1 coherence across behavioral conditions. Optogenetic experiments and excitatory-inhibitory network simulations identified afferent synaptic inputs rather than spiking entrainment as the principal determinant of coherence. These findings suggest that unique spectral profiles of different brain areas automatically give rise to large-scale coherence patterns that follow anatomical connectivity and continuously reconfigure as a function of behavior and cognition.

A Distinct Class of Bursting Neurons with Strong Gamma Synchronization and Stimulus Selectivity in Monkey V1.

Cortical computation depends on interactions between excitatory and inhibitory neurons. The contributions of distinct neuron types to sensory processing and network synchronization in primate visual cortex remain largely undetermined. We show that in awake monkey V1, there exists a distinct cell type (>>30% of neurons) that has narrow-waveform (NW) action potentials and high spontaneous discharge rates and fires in high-frequency bursts. These neurons are more stimulus selective and phase locked to 30- to 80-Hz gamma oscillations than other neuron types. Unlike other neuron types, their gamma-phase locking is highly predictive of orientation tuning. We find evidence for strong rhythmic inhibition in these neurons, suggesting that they interact with interneurons to act as excitatory pacemakers for the V1 gamma rhythm. We did not find a similar class of NW bursting neurons in L2-L4 of mouse V1. Given its properties, this class of NW bursting neurons should be pivotal for the encoding and transmission of stimulus information.

Surface color and predictability determine contextual modulation of V1 firing and gamma oscillations.

The integration of direct bottom-up inputs with contextual information is a core feature of neocortical circuits. In area V1, neurons may reduce their firing rates when their receptive field input can be predicted by spatial context. Gamma-synchronized (30-80 Hz) firing may provide a complementary signal to rates, reflecting stronger synchronization between neuronal populations receiving mutually predictable inputs. We show that large uniform surfaces, which have high spatial predictability, strongly suppressed firing yet induced prominent gamma synchronization in macaque V1, particularly when they were colored. Yet, chromatic mismatches between center and surround, breaking predictability, strongly reduced gamma synchronization while increasing firing rates. Differences between responses to different colors, including strong gamma-responses to red, arose from stimulus adaptation to a full-screen background, suggesting prominent differences in adaptation between M- and L-cone signaling pathways. Thus, synchrony signaled whether RF inputs were predicted from spatial context, while firing rates increased when stimuli were unpredicted from context.

A Functional Gradient in the Rodent Prefrontal Cortex Supports Behavioral Inhibition.

The ability to plan and execute appropriately timed responses to external stimuli is based on a well-orchestrated balance between movement initiation and inhibition. In impulse control disorders involving the prefrontal cortex (PFC) [1], this balance is disturbed, emphasizing the critical role that PFC plays in appropriately timing actions [2-4]. Here, we employed optogenetic and electrophysiological techniques to systematically analyze the functional role of five key subareas of the rat medial PFC (mPFC) and orbitofrontal cortex (OFC) in action control [5-9]. Inactivation of mPFC subareas induced drastic changes in performance, namely an increase (prelimbic cortex, PL) or decrease (infralimbic cortex, IL) of premature responses. Additionally, electrophysiology revealed a significant decrease in neuronal activity of a PL subpopulation prior to premature responses. In contrast, inhibition of OFC subareas (mainly the ventral OFC, i.e., VO) significantly impaired the ability to respond rapidly after external cues. Consistent with these findings, mPFC activity during response preparation predicted trial outcomes and reaction times significantly better than OFC activity. These data support the concept of opposing roles of IL and PL in directing proactive behavior and argue for an involvement of OFC in predominantly reactive movement control. By attributing defined roles to rodent PFC sections, this study contributes to a deeper understanding of the functional heterogeneity of this brain area and thus may guide medically relevant studies of PFC-associated impulse control disorders in this animal model for neural disorders [10-12].