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Brain of the Japanese carpenter ant (Camponotus japonicus)


Michiko Nishikawa (Fukuoka University
)


Brain structure of a carpenter ant

The Japanese carpenter ant (Camponotus japonicus) is a social insect belonging to the order Hymenoptera, along with the honey bee. Their colonies comprise two distinct castes, reproductive ants, including males and females, and non-reproductive ants, including worker ants that are genetically female but sterile. The females are approximately 2 cm in length, and the males have a length of approximately 1 cm. The size of worker ants is in the range 1–2 cm (Fig. 1). During the spring mating season, winged male and female ants appear near the entrance of the nest, and fly out on the wedding flight. While males that have completed aerial mating die, the mated females return to land, drop their wings, dig a new nest, and lay eggs. The larvae that hatch first become worker ants; they are responsible for the care and feeding of other larvae. The mated female focuses on laying eggs and founds the colony as the queen ant (Fig. 2). Each caste in the colony has its own special role in the division of labor; this is reflected in their brain structures. The neuropil in the brain is the site of synaptic connection between neurons where information is received, and its constitution is universal among insect brains. The main neuropil in the brain includes the optic lobes, receiving visual information from the compound eyes; the antennal lobes, receiving olfactory information from the antennae; and the mushroom bodies as the higher order association center, integrating pieces of sensory information (each as a pair in the left and right hemispheres), and the central complex at the center of two hemispheres, which is associated with orientation and flight. The brain situates above the esophagus, while the subesophageal ganglion beneath the esophagus receives sensory information from mouth appendages (Fig. 3). A three-dimensional structure of the neuropil constructed on the basis of optical sections of the brain obtained using a confocal laser scanning microscope (LSM) with a three-dimensional construction software (Fig. 4), which allows calculation of the volume of each neuropil. Results show that, although the large females have the maximum neuropil volume for all neuropils (Fig. 5), the ratio of the volume of each neuropil to the total brain volume reflects the different performance characteristics of the castes (Fig. 6). The male ants, which do not perform any task inside the colony and specialize in mating behavior during the wedding flight, show relatively large ratios of the optic lobes and central complex related to visual information processing compared with females and worker ants. In contrast, female and worker ants, which play roles in forming and maintaining the colony, have larger ratios of the antennal lobes and mushroom bodies related to processing of sensory information from antennae, compared with male ants. The neuropil ratios also differ between female and worker ants depending on their roles. Female ants participate in wedding flights; therefore, the optic lobe ratio is higher than in workers. Because of the responsibilities of worker ants in maintaining the colony, the mushroom body, with its connection to sensory integration and learning, has a larger ratio compared with the female ants (Fig. 6). When brains of the Japanese carpenter ants were immunostained with serotonin antibodies, an extremely large number of serotonin-positive neurons were stained (Fig. 7, video 1). Among them, three types of serotonin-positive neurons with neurites in the neuropil involved in the processing of olfactory information such as the antennal lobe glomeruli, the mushroom body calyx, and the lateral horn have been morphologically identified (Fig. 7). These neurons are believed to play certain roles in olfactory information processing.




Fig. 1.Japanese carpenter ant (adapted from Tsuji et al., 2007)
From left: worker ant, female ant (the queen ant, after mating), and male ant.




Fig. 2.Japanese carpenter ants in a terrarium
From left: queen ant, worker ant, and pupa.




Fig. 3. Cross-sections of the brain of a Japanese carpenter ant
Vertical (left) and sagittal cross-sections (right) of worker ant brains stained with ethyl gallate.
AL, antennal lobe; CC, central complex; DL, dorsal lobe; la, lamina; lCa, lateral calyx; ld, lower division; lo, lobula; LP, lateral protocerebrum; M, medial; MB, mushroom body; mCa, medial calyx; me, medulla; mL, medial lobe; OL, optic lobe; Pe, peduncle; SEG, subesophageal ganglion; ud, upper division; V, ventral; vL, vertical lobe.




Fig. 4. Constructed three-dimensional structure of the brain neuropil in the Japanese carpenter ant
(adapted from Nishikawa et al., 2008)
From left: worker ant, female ant, male, and brain. Abbreviations as in Fig. 3.




Fig. 5. Volumes ofthe neuropiles in the brain(Nishikawa et al., 2008 Modified)
AL, antennal lobe; Br/SEG, brain/subesophageal ganglion; CC, central complex; MB, mushroom body; OL, optic lobe .





Fig. 6. Relative volumes of the neuropiles in the brain(Nishikawa et al., 2008 Modified)
Relative values of the neuripiles are shonw with respect to that of Br/SE.
AL, antennal lobe; CC, central complex; MB, mushroom body; OL, optic lobe .




Fig. 7. Serotonin-positive neurons in the brain of the Japanese carpenter ant. Anti-serotonin immunostaining image (a) and three types of serotonin-positive neurons with neurites in the neuropil involved in olfactory information processing (b–d) in the brain of Japanese carpenter worker ant. b. The soma is located in the dorso-medial region of the protocerebrum and sends neurites into the lateral horn of the ipsilateral hemisphere, the lip of the mushroom body calyx and the lateral horn of the contralateral hemisphere. c. The soma is not specifically located, but a thick axon derived from the subesophageal ganglion sends neurites into ipsilateral antennal lobe glomeruli. d. The soma is located in the lateral cell body group of the antennal lobe, sends neurites into approximately 10 glomeruli in the dorsal region of the antennal lobe, and the lateral horn of the protocerebrum in the ipsilateral hemisphere, and the dorso-medial region of the protocerebrum in the contralateral hemisphere.
AL, antennal lobe; SEG, subesophageal ganglion; CC, central complex; MB, mushroom body; OL, optic lobe.(Tsuji et al., 2007)


References

Nishikawa M, Nishino H, Misaka Y, Kubota M, Tsuji E, Satoji Y, Ozaki M, Yokohari F. (2008) Sexual dimorphism in the antennal lobe of the ant Camponotus japonicus. Zoolog Sci. 25(2):195-204.

Tsuji E, Aonuma H, Yokohari F, Nishikawa M. (2007) Serotonin-immunoreactive neurons in the antennal sensory system of the brain in the carpenter ant, Camponotus japonicus. Zool Sci 24:836-849.


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