From a brain's-eye-view, when a stimulus occurs and what it is are interrelated aspects of interpreting the perceptual world. Yet in practice, the putative perceptual inferences about sensory content and timing are often dichotomized and not investigated as an integrated process. We here argue that neural temporal dynamics can influence what is perceived, and in turn, stimulus content can influence the time at which perception is achieved. This computational principle results from the highly interdependent relationship of what and when in the environment. Both brain processes and perceptual events display strong temporal variability that is not always modeled; we argue that understanding—and, minimally, modeling—this temporal variability is key for theories of how the brain generates unified and consistent neural representations and that we ignore temporal variability in our analysis practice at the peril of both data interpretation and theory-building. Here, we review what and when interactions in the brain, demonstrate via simulations how temporal variability can result in misguided interpretations and conclusions, and outline how to integrate and synthesize what and when in theories and models of brain computation.

Hierarchical structure and compositionality imbue human language with unparalleled expressive power and set it apart from other perception–action systems. However, neither formal nor neurobiological models account for how these defining computational properties might arise in a physiological system. I attempt to reconcile hierarchy and compositionality with principles from cell assembly computation in neuroscience; the result is an emerging theory of how the brain could convert distributed perceptual representations into hierarchical structures across multiple timescales while representing interpretable incremental stages of (de)compositional meaning. The model's architecture—a multidimensional coordinate system based on neurophysiological models of sensory processing—proposes that a manifold of neural trajectories encodes sensory, motor, and abstract linguistic states. Gain modulation, including inhibition, tunes the path in the manifold in accordance with behavior and is how latent structure is inferred. As a consequence, predictive information about upcoming sensory input during production and comprehension is available without a separate operation. The proposed processing mechanism is synthesized from current models of neural entrainment to speech, concepts from systems neuroscience and category theory, and a symbolic-connectionist computational model that uses time and rhythm to structure information. I build on evidence from cognitive neuroscience and computational modeling that suggests a formal and mechanistic alignment between structure building and neural oscillations, and moves toward unifying basic insights from linguistics and psycholinguistics with the currency of neural computation.

The ability to use words to refer to the world is vital to the communicative power of human language. In particular, the anaphoric use of words to refer to previously mentioned concepts (antecedents) allows dialogue to be coherent and meaningful. Psycholinguistic theory posits that anaphor comprehension involves reactivating a memory representation of the antecedent. Whereas this implies the involvement of recognition memory or the mnemonic subroutines by which people distinguish old from new, the neural processes for reference resolution are largely unknown. Here, we report time–frequency analysis of four EEG experiments to reveal the increased coupling of functional neural systems associated with referentially coherent expressions compared with referentially problematic expressions. Despite varying in modality, language, and type of referential expression, all experiments showed larger gamma-band power for referentially coherent expressions compared with referentially problematic expressions. Beamformer analysis in high-density Experiment 4 localized the gamma-band increase to posterior parietal cortex around 400–600 msec after anaphor onset and to frontotemporal cortex around 500–1000 msec. We argue that the observed gamma-band power increases reflect successful referential binding and resolution, which links incoming information to antecedents through an interaction between the brain's recognition memory networks and frontotemporal language network. We integrate these findings with previous results from patient and neuroimaging studies, and we outline a nascent corticohippocampal theory of reference.