A mechanosensory feedback that uncouples external and self-generated sensory responses in the olfactory cortex

Abstract

A fundamental problem for any sensory system is that the motion of the sensory organ introduces a disturbance in sensory measurement. Nevertheless, animal nervous systems can distinguish and compensate for the sensory consequences of movement by keeping track of them. Hypotheses for estimating the motion of a sensory organ include a corollary discharge associated with motor output and mechanosensory inputs from the moving sense organ. However, how motion-related mechanosensory inputs can reduce motion-dependent sensory ambiguity is unknown. We addressed this question in the olfactory system, where changes in inhalation dynamics alter the sorption of odor molecules by the nasal mucosa and mechanically activate olfactory sensory neurons. We found that changes in inhalation dynamics varied the odor concentration reported by the individual neurons in the piriform cortex. However, the actual odor concentration could be decoded from the population activity regardless of the inhalation dynamics. Dynamics-invariant decoding was possible because piriform cortex neurons have a heterogeneously mixed sensitivity for odor concentration and inhalation dynamics. Thus, the mechanosensory input generated by inhalation expanded the dimensionality of the olfactory encoding space and disentangled the decoding of the actual odor concentration from the disturbance caused by the sniff. Orthogonal integration of motion-related mechanosensory information during the encoding stage may be a canonical strategy adopted by nervous systems to mitigate the sensory ambiguities generated by the motion of the sensory organ.