Convergence of mechanosensory afferents from different classes of exteroceptors onto spiking local interneurons in the locust

Abstract

Tactile stimuli to a leg of a locust are detected by two classes of exteroceptors: trichoid sensilla (tactile hairs), which are purely mechanoreceptors, and basiconic sensilla, which serve a dual role as mechano- and chemoreceptors. The trichoid sensilla have the longer shafts, but because the two types of receptors are intermingled over the surface of a leg, both can be excited when the leg contacts an obstacle. This article analyzes the mechanisms by which the tactile sensory information from these two classes of receptor is collated in the CNS so that spatial information is preserved. The mechanosensory afferents from both types of receptors on a hind leg make convergent connections that are excitatory and apparently direct with the same spiking local interneurons in a midline population of the metathoracic ganglion. The anatomy of the afferent projections suggests that the synapses from the two types of receptor are made onto the same region of branches of an interneuron. The slower conduction velocity of the spikes of the basiconic afferents compared to that of the trichoid afferents means that a mechanical stimulus to the tibia will first produce a depolarization caused by the trichoid afferents, followed up to 20 msec later by a depolarization caused by the basiconic sensilla. Each interneuron is excited by a contiguous and overlapping array of trichoid and basiconic receptors that form its receptive field. Different interneurons have different receptive fields such that the surface of the leg is mapped as a series of overlapping receptive fields. Within a receptive field the contribution of individual receptors can be markedly different: some basiconic receptors evoke large-amplitude EPSPs so that each afferent spike can cause a spike in the interneuron, whereas others generate small EPSPs that must sum with other inputs to evoke a spike. The amplitudes of the EPSPs generated by different receptors within a receptive field form gradients that are distributed according to the axes of the leg. The most effective basiconic and the most effective trichoid sensilla within a particular receptive field can be at the same or at different locations on the leg. Tactile sensory information from different types of receptor on one region of a leg is therefore collated initially by particular spiking local interneurons. This organization ensures summation between the inputs from the different types of receptors and should enhance sensitivity. It also preserves spatial information for use in tactile reflexes, and could ensure that appropriately directed movements are made in response to the parallel information from the chemosensory afferents that innervate the basiconic sensilla.