This paper considers neuronal architectures from a computational perspective and asks what aspects of neuroanatomy and neurophysiology can be disclosed by the nature of neuronal computations? In particular, we extend current formulations of the brain as an organ of inference—based upon hierarchical predictive coding—and consider how these inferences are orchestrated. In other words, what would the brain require to dynamically coordinate and contextualize its message passing to optimize its computational goals? The answer that emerges rests on the delicate (modulatory) gain control of neuronal populations that select and coordinate (prediction error) signals that ascend cortical hierarchies. This is important because it speaks to a hierarchical anatomy of extrinsic (between region) connections that form two distinct classes, namely a class of driving (first-order) connections that are concerned with encoding the content of neuronal representations and a class of modulatory (second-order) connections that establish context—in the form of the salience or precision ascribed to content. We explore the implications of this distinction from a formal perspective (using simulations of feature–ground segregation) and consider the neurobiological substrates of the ensuing precision-engineered dynamics, with a special focus on the pulvinar and attention.

When we recognize a sensory event, we experience a confident feeling that we certainly know the perceived world 'here and now'. However, it is unknown how and where the brain generates such 'perceptual confidence'. Here we found neural correlates of confidence in the primate pulvinar, a visual thalamic nucleus that has been expanding markedly through evolution. During a categorization task, the majority of pulvinar responses did not correlate with any 'perceptual content'. During an opt-out task, pulvinar responses decreased when monkeys chose 'escape' options, suggesting less confidence in their perceptual categorization. Functional silencing of the pulvinar increased monkeys' escape choices in the opt-out task without affecting categorization performance; this effect was specific to the contralateral visual target. These data were supported by a theoretical model of confidence, indicating that pulvinar activities encode a subject's certainty of visual categorization and contribute to perceptual confidence.