The neuroanatomy of nitric oxide-cyclic GMP signaling in the locust: functional implications for sensory systems'

Abstract

SYNOPSIS. Recent studies have investigated the source and target neurons for the diffusible neuronal messenger molecule nitric oxide (NO) in the nervous system of the locust. Here \ve compare the neuroarchitecture of NO signaling between different sensory systems. The available neuroanatomical data implicate NO in sensory processing for modalities as diverse as mechanoreception, vision, olfaction, gustation and hearing. All respective first-order sensory neuropils are innervated by NOS-containing interneurons. The corresponding sensory receptor neurons lack NOS but seem to express soluble guanylyl cyclase (sGC), the main receptor molecule, for NO in the nervous system. The axonal projections of sensory neurons must therefore be considered the primary target of NO in these sensory neuropils. An exception is the antennal olfactory system where sGC is apparently expressed in interneurons, in partial colocalization with NOS. We discuss these anatomical findings in relation to the spatiotcmporal characteristics of NO signaling. Many sensory neuropils are organized into maps that reflect neuronal response properties (i.e., tuning or receptive fields). A local release of NO within such maps will therefore most strongly affect neurons with similar coding properties. If sensory receptor activity triggers NO synthesis locally in the map, this mechanism could link groups of similarly tuned receptors dynamically according to stimulus intensity. Furthermore, we explore the functional implications of differences between sensory systems in the anatomy of NOS-expressing interneurons, using the compound eye and the thoracic tactile system as examples.