Mosaic organization of body pattern control in the optic lobe of squids

Abstract

Cephalopods in nature undergo highly dynamic skin coloration changes that allow rapid camouflage and intra-species communication. The optic lobe is thought to play a key role in controlling the expansion of the chromatophores that generate these diverse body patterns. However, the functional organization of the optic lobe and neural control of the various body patterns by the optic lobe are largely unknown. We applied electrical stimulation within the optic lobe to investigate the neural basis of body patterning in the oval squid Sepioteuthis lessoniana. Most areas in the optic lobe mediated predominately ipsilateral expansion of chromatophores present on the mantle but not on the head and arms; furthermore, the expanded areas after electrical stimulation were positively correlated with an increase in stimulating voltage and stimulation depth. These results suggest a unilaterally dominant and vertically converged organization of the optic lobe. Furthermore, analyzing fourteen of the elicited body pattern components and their corresponding stimulation sites revealed that the same components can be elicited by stimulating different parts of the optic lobe and that various subsets of these components can be co-activated by stimulating the same area. These findings suggest that many body pattern components may have multiple motor units in the optic lobe and these are organized in a mosaic manner. The multiplicity associated with the nature of the neural controls of these components in the cephalopod brain thus reflects the versatility of the individual components during the generation of diverse body patterns.

SIGNIFICANCE STATEMENT

Neural control of the dynamic body patterning of cephalopods for camouflage and intra-species communication is a fascinating research topic. Previous studies have shown that the optic lobe is the motor command center for dynamic body patterning. However, little is known about its neural organization and the mechanisms underlying its control of body pattern generation. By electrically stimulating the optic lobe of the oval squids and observing their body pattern changes, surprisingly, we found that there is no somatotopic organization of motor units. Instead, many of these components have multiple motor units within the optic lobe and that they are organized in a mosaic manner. The present work reveals a novel neural control of dynamic body patterning for communication in cephalopods.