Neural regulation of a complex behavior: body patterning in cephalopod molluscs

Abstract

Unshelled cephalopods have a remarkable ability to alter their appearance, using textural, postural, and chromatic elements to generate a myriad of body patterns. Of the unshelled cephalopods, it is generally acknowledged that cuttlefish express the most detailed and widest range of body patterns, including static and dynamic patterns. In this paper we present data on the neuronal mechanisms underlying this amazing behavior, focusing on the neuroregulation of the chromatic elements, the chromatophore organs, in the European cuttlefish Sepia officinalis. Cephalopod chromatophore organs, including those in Sepia, are unlike those in any other animal taxa; each consists of a pigment-containing chromatophore cell that expands in response to the coordinated activation of a set of radial muscles which are directly attached to the chromatophore cell. We show that the chromatophore muscles are regulated by 2 different excitatory transmitters, glutamate and the family of FMRFamide-related peptides (FaRPs). Glutamate mediates rapid and transient chromatophore cell expansion whereas the FaRPs are responsible for slower, more sustained responses. Using retrograde dye filling, immunocytochemical and in situ hybridization techniques, we demonstrate that the cell bodies of the glutamatergic and FaRPs-containing motoneurons innervating the fin chromatophore muscles are primarily localized to the posterior chromatophore and fin lobes in the posterior subesophageal mass of the Sepia brain. Data are also presented showing that some fin chromatophore motoneurons have multiple axons in different nerve branches, which accounts for overlapping chromatophore motor fields by adjacent peripheral nerves.