Differential rapid plasticity in auditory and visual responses in the primarily multisensory orbitofrontal cortex

Abstract

AbstractIn a dynamic environment with rapidly changing contingencies, the orbitofrontal cortex (OFC) guides flexible behavior through coding of stimulus value. Although stimulus-evoked responses in the OFC are known to convey outcome, baseline sensory response properties in the mouse OFC are poorly understood. To understand mechanisms involved in stimulus value/outcome encoding it is important to know the response properties of single neurons in the mouse OFC, purely from a sensory perspective. Ruling out effects of behavioral state, memory and others, we studied the anesthetized mouse OFC responses to auditory, visual and audiovisual/multisensory stimuli, multisensory associations and sensory-driven input organization to the OFC. Almost all, OFC single neurons were found to be multisensory in nature, with sublinear to supralinear integration of the component unisensory stimuli. With a novel multisensory oddball stimulus set, we show that the OFC receives both unisensory as well as multisensory inputs, further corroborated by retrograde tracers showing labeling in secondary auditory and visual cortices, which we find to also have similar multisensory integration and responses. With long audiovisual pairing/association, we show rapid plasticity in OFC single neurons, with a strong visual bias, leading to a strong depression of auditory responses and effective enhancement of visual responses. Such rapid multisensory association driven plasticity is absent in the auditory and visual cortices, suggesting its emergence in the OFC. Based on the above results we propose a hypothetical local circuit model in the OFC that integrates auditory and visual information which participates in computing stimulus value in dynamic multisensory environments.Significance StatementProperties and modification of sensory responses of neurons in the orbitofrontal cortex (OFC) involved in flexible behavior through stimulus value/outcome encoding are poorly understood. Such responses are critical in providing the framework for the encoding of stimulus value based on behavioral context while also directing plastic changes in sensory regions. The mouse OFC is found to be primarily multisensory with varied nonlinear interactions, explained by unisensory and multisensory inputs. Audio-visual associations cause rapid plastic changes in the OFC, which bias visual responses while suppressing auditory responses. Similar plasticity was absent in the sensory cortex. Thus the observed intrinsic visual bias in the OFC weighs visual stimuli more than associated auditory stimuli in value encoding in a dynamic multisensory environment.