Central distribution and three-dimensional arrangement of fin chromatophore motoneurons in the cuttlefish Sepia officinalis

Abstract

Cephalopod body patterning is a most complex invertebrate behavior. Generated primarily by pigment-containing chromatophore organs, this behavior enables rapid alteration of body coloration as a result of direct innervation of chromatophores by motoneurons. This study focuses on location and arrangement of fin chromatophore motoneurons in the cuttlefish Sepia and investigates the possibility of central topography. Retrograde labeling of topographically arranged fin nerve branches in the periphery revealed the posterior subesophageal mass (PSEM) of the brain as the primary location of fin chromatophore motoneurons; within this region, most cells were located in the posterior chromatophore and fin lobes. Additionally, a small percentage of labeled motoneurons occurred in the anterior subesophageal mass and the stellate ganglia. Data from three-dimensional reconstructions of PSEMs showed the arrangement of labeled motoneurons within individual lobes; these data suggest no obvious topographic arrangement. Further, electrical stimulation of the PSEM generated chromatophore activity on the fin and mantle. These stimulation results, coupled with the retrograde labeling, suggest that chromatophore motoneurons are located across multiple PSEM lobes.

Characterization of Homeobox Genes Reveals Sophisticated Regionalization of the Central Nervous System in the European Cuttlefish Sepia officinalis

“…The combination of Lhx3/4 and islet, another LIM-class homeodomain protein, is necessary for motor neuron specification in Drosophila [11] and vertebrates (chick: [10] ; zebrafish: [8] ). No data is currently available regarding islet expression in cephalopods, however analysis of chromatophore motor neuron distribution reveals the SM, in particular the pSM, as a sight of concentrated motor neurons [41] [42] , confirming earlier reports of motor activity in response to electrical stimulation in these lobes [39] . Here we find that Sof-Lhx3-4 is broadly expressed throughout the nervous system of the cuttlefish, including the anterior-most portion of the mSM and aSM, potentially overlapping with so-Mnx expression domains ( Figure 6 , [26] ) and thus suggesting the presence of a conserved motor neuron molecular signature in cephalopods.…”

Cephalopod Brains: An Overview of Current Knowledge to Facilitate Comparison With Vertebrates

“…However, a somatotopic map has been suggested to occur in the sub-esophageal mass (e.g., Boycott, 1961 ; Monsell, 1980 ; Saidel, 1981 ; Dubas et al, 1986 ; Gaston and Tublitz, 2004 ; Gaston and Tublitz, 2006 ). A multi-color neuro-tracing study of the central distribution and the resulting three-dimensional arrangement of fin chromatophore motoneurons in the cuttlefish ( Gaston and Tublitz, 2006 ), provided preliminary possible topographic organization of fin chromatophore motoneurons. These data support previous findings by Boycott (1961) who proposed a type of ‘somatotopy’ when considering the neural representation (in the chromatophore lobes, SUB) of chromatophores in the skin of the animals, depending on the species.…”

“…Along the D–V axis (as depicted above for cephalopod brain), centers characterizing the sub-esophageal mass and controlling specific body parts are arranged in the same order as those body parts: the pallial cavity, then the viscera, collar, funnel, head, ocular system, oculomotor system, and finally arms ( Young, 1976a ; Budelmann and Young, 1985 ; Gaston and Tublitz, 2006 ; Figure 4 ). However, and based on the available knowledge, neuronal segregation of the ventral motor and dorsal sensory neurons has not been reported for cephalopod sub-esophageal mass, and an analogy with the vertebrate arrangement seems difficult.…”

Chromatophore Activity during Natural Pattern Expression by the Squid Sepioteuthis lessoniana: Contributions of Miniature Oscillation

“…The patterns are mediated by retraction and expansion of chromatophore organs (referred to hereafter as chromatophore(s)). A chromatophore consists of a central pigment-containing cell surrounded by 19–27 radial muscles that are controlled by motor neurons in the brain [2], [3], [4], [5]. Contraction of the radial muscles causes an expansion of the pigment-containing cell.…”