Sequential and dynamic coding of water-sucrose categorization in rat gustatory cortices

Abstract

The gustatory system underlies our conscious perception of sweetness and allows us to distinguish a sweet solution from plain water. However, the neural mechanisms in gustatory cortices that enable rats to differentiate sweetness from water remain elusive. In this study, we designed a novel sucrose categorization task in which rats classified water from a gradient of sucrose solutions. We found that in the anterior Insular Cortex (aIC) and the Orbitofrontal Cortex (OFC), neural activity prioritized encoding the categorization of water versus sucrose rather than the specific concentrations within the sucrose solutions. aIC neurons more rapidly encoded sucrose/water distinction, followed by the OFC. In contrast, the OFC encoded choice information slightly earlier than aIC, but both gustatory cortices maintained a comparable encoding of the rat's choices in parallel. The encoding of sensory and categorical decisions was dynamic and sequentially encoded, with neurons carrying significant information in moving bumps at different time bins across the trial. Our results demonstrate that sucrose categorization relies on dynamic encoding sequences in the neuronal activity of aIC and the OFC rather than static, long-lasting (sustained) neural representations. Single-cell, population decoding, and principal component analyses confirmed our results. This aligns with the concept of a dynamic code, where the brain updates its representation of sucrose categorization as new information becomes available. Additionally, aIC and the OFC rapidly encoded reward outcomes. Our data supports the view that gustatory cortices use sequential and dynamic coding to compute sensorimotor transformations from taste detection to encoding categorical taste decisions and reward outcomes.