Extraction of Sensory Parameters from a Neural Map by Primary Sensory Interneurons

We examine the anatomical basis for the representation of stimulus parameters within a neural map and examine the extraction of these parameters by sensory interneurons (INs) in the cricket cercal sensory system. The extraction of air current direction by these sensory interneurons can be understood largely in terms of the anatomy of the system. There are two critical anatomical constraints. (1) The arborizations of afferents with similar directional tuning properties are located near each other within the neural map. Therefore, a continuous variation in stimulus direction causes a continuous variation in the spatial pattern of activation. (2) The restriction of the synaptic connections of an interneuron to a unique set of afferents results from the unique anatomy of that interneuron: its dendritic arbors are located within restricted regions of the afferent map containing afferents with a limited subset of directional sensitivities. The functional organization of the set of four interneurons studied here is equivalent to a Cartesian coordinate system for computing the stimulus direction vector. For any air current stimulus direction, the firing rates of the active interneurons could be decoded as Cartesian coordinates by neurons at successive processing stages. The implications of this Cartesian coordinate system are discussed with respect to optimal coding strategies and developmental constraints on the cellular implementation of this coding scheme.