Somatosensory modulation of visual cortex responses during trace conditioning under anesthesia

Learning and memory enables organisms to make predictions about the outcomes associated with specific stimuli. Although anesthesia inhibits the formation of explicit memories, it does not hinder the formation of implicit memories (Samuel et al., 2018).The neural mechanisms underlying implicit learning and memory formation under anesthesia are understudied, especially for multisensory associations. We recorded neural activity in early visual cortex of rhesus macaques under propofol anesthesia to determine how neuronal responses are modulated during a trace conditioning procedure in which naturalistic visual stimuli were flickered at 10 Hz (CS; e.g. faces, objects, and symmetrical visual textures) and probabilistically associated with delayed somatosensory stimulation of the fingers (US). One set of visual cues was associated with a high probability of somatosensory stimulation while the other was associated with a low probability. Pupillometry was used to verify that conditioned associations were learned (n = 5). Trial-by-trial changes in the predictability of each cue to signal subsequent somatosensory stimulation were encoded by changes in pupil size. The most prominent outcome was pupillary constriction immediately after experiencing somatosensory US, regardless of whether it was preceded by a high or low probability visual cue. Multi-contact neurophysiology probes were used to record in areas V1, V2, and V4 (n = 3). In each area, 30-50% of the recorded neurons exhibited modulations in ongoing neural responses elicited by the flickering visual cues depending on whether the somatosensory US was delivered. Complementary experiments used intrinsic optical imaging (IOI) to measure changes in neural activation at the mesoscale similarly found somatosensory related modulation of hemodynamic responses in areas V1, V2, and V4. These results imply that under anesthesia implicit multisensory associations can modulate early visual cortical responses. These findings provide a framework to a better understand the neural circuitry underlying implicit learning and the neurocognitive adverse effects of anesthesia.