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Distribution of Glutamic Acid Decarboxylase Immunoreactivity Within the Brain of Oval Squid Sepioteuthis Lessoniana

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Distribution of Glutamic Acid Decarboxylase Immunoreactivity Within the Brain of Oval Squid Sepioteuthis Lessoniana Vol. 19: 97–109, 2013 AQUATIC BIOLOGY Published online September 24 doi: 10.3354/ab00525 Aquat Biol OPENPEN ACCESSCCESS FEATURE ARTICLE Distribution of glutamic acid decarboxylase immunoreactivity within the brain of oval squid Sepioteuthis lessoniana Shiori Kobayashi1, Chitoshi Takayama2, Yuzuru Ikeda1,* 1Department of Marine and Environmental Sciences, Graduate School of Engineering and Science, and 2Department of Molecular Anatomy, Graduate School of Medicine, University of the Ryukyus, Okinawa 903-0213, Japan ABSTRACT: Coleoid cephalopods (squid, cuttlefish, and octopus) have the largest and most complex brains of all invertebrates and show behavioral abilities similar to those of vertebrates. Among the coleoids, the oval squid Sepioteuthis lessoniana forms well-structured schools that are indicative of sociality. These behaviors are re flected in aspects of the well-developed brain. In this study, we focused on the role of the cephalopod brain in complex behavior. In order to reveal the network of γ-aminobutyric acid (GABA) in coleoids, we examined the immunohistochemical localization of glutamic acid decarboxylase (GAD), which is the synthetic enzyme of GABA, in the brain of young Oval squid Sepioteuthis lessoniana demonstrating social behaviour. S. lessoniana. We found that GABAergic neurons Photo: Ryuta Nakajima and their axons were distributed throughout the brain. GABA neurons were abundantly localized in the inferior frontal lobe, which is involved in controlling arm motions, and in the subesophageal INTRODUCTION masses, which are lower and intermediate centers of action. GABAergic fibers were abundantly The coleoid cephalopod mollusks (squid, cuttlefish, localized in the tract that runs from the superior and octopus) have elaborate sense organs and cen- frontal lobe to the vertical lobe. These results sug- tral nervous systems (CNS) that are the most complex gested the involvement of GABA in both cognitive among invertebrates (Budelmann 1995). The relative behaviors (such as learning and memory) and in volume of the coleoid cephalopod CNS is larger than movement. that of phylogenetically lower vertebrates such as KEY WORDS: Glutamic acid decarboxylase · fishes and reptiles, but smaller than that of higher Neurotransmitter · Brain · Oval squid · GABA · vertebrates such as mammals and birds (Packard γ-aminobutyric acid 1972). The complex and large CNS enables these animals to adapt to various oceanic environments. Cephalopods are competitive counterparts of fish, © The authors 2013. Open Access under Creative Commons by *Corresponding author. Email: [email protected] Attribution Licence. Use, distribution and reproduction are un - restricted. Authors and original publication must be credited. Publisher: Inter-Research · www.int-res.com 98 Aquat Biol 19: 97–109, 2013 and live in various types of marine environments the CNS: γ-aminobutyric acid (GABA). GABA is the where they are active predators and migrators, capa- major inhibitory neurotransmitter in both vertebrates ble of moving quickly. Cephalopods’ remarkable and invertebrates (Jackson et al. 1990, Lunt 1991, behavioral and cognitive abilities include learning Nishimura et al. 2008), and is highly conserved in processes (e.g. reversal, observational, and spatial evolution; it has been suggested that GABA plays a learning) that are equivalent to those observed in role in various higher functions in the brain of the many vertebrates (Hanlon & Messenger 1996). In common cuttlefish Sepia officinalis and common octo- spite of their short lifespan (from 1 to 2 yr) cephalo - pus Octopus vulgaris (Tsukada et al. 1964, Cornwell pods are equipped with major sense organs, includ- et al. 1993, D’Aniello et al. 1995). In adult vertebrates, ing human-like lens eyes. These advanced features GABAergic neurons play important roles in a variety are considered to be a consequence of coevolution of states and physiological processes, including inhi- with their rivals—marine vertebrates such as fish bition of anxiety, walking, circadian rhythms, and (Packard 1972). Considering these characteristics, emotional responses (Stork et al. 2000, Miczek et al. the cephalopod brain has been the subject of many 2002). Physiological and pharmacological studies investigations of brain mechanisms that underlie have reported that GABA is both excitatory and in- behavioral plasticity (Hochner et al. 2006). hibitory for neurons in the CNS and is involved in ac- The oval squid Sepioteuthis lessoniana is a nektonic tivating feeding movements via buccal and cerebral animal that is widely distributed throughout the shal- ganglion neurons in mollusks (Cooke & Gelperin 1988, low waters of the Indian and West Atlantic Oceans. Rich mond et al. 1991, 1994, Arshavsky et al. 1993, Oval squid have 2 specific behavioral characteristics Hernádi 1994, Hatakeyama & Ito 2000, Elliott & Suss- that other cephalopods do not have. One of these wein 2002). The presence of GABA was investigated unique characteristics is that they form a well-struc- in cephalo pods by Tansey (1979) and Cornwell et al. tured school. It has been reported that the Caribbean (1993), and conflicting evidence has been presented reef squid, S. sepioidea, which is phylo genetically regarding the presence of GABA in the cephalopod close to S. lessoniana, exhibits social in teractions CNS (Tansey 1979). Cornwell et al. (1993) demon- within shoals in which each member is arranged in a strated widespread GABA-like staining in the many definite order with one individual acting as a sentinel brain lobes of the Eledone. In the present study, we (Moynihan & Rodaniche 1982). A similar type of re-examined the existence and distribution of GABA - schooling behavior appears in S. lessoniana up to 2 ergic elements in the CNS of Sepioteuthis lessoniana. months after hatching, at which age squids are To detect the GABAergic system, we performed im- thought to become capable of recognizing school- munohistochemistry for glutamic acid decarboxylase mates (Sugimoto & Ikeda 2012). The second charac- (GAD), which is the synthetic enzyme of GABA and teristic unique to the oval squid is the capacity to a marker protein of GABA neurons in young squid. change its body color (termed ‘body pattern’) very quickly. Body patterns are involved in many aspects of coleoid life, including courtship, communication, MATERIALS AND METHODS camouflage, and predator–prey relationships (Hanlon & Messenger 1996). These characteristics indicate the Egg collection and rearing of paralarvae possibility that S. lessoniana have sociality. Previous studies have demonstrated the cytoarchitecture of the Egg capsules of Sepioteuthis lessoniana spawned CNS of adult and embryonic squids and paralarvae on set nets were collected from Nago Bay of the Oki- (Meister 1972, Young 1974, 1976, 1977, 1979, Mes- nawa Islands, Okinawa, Japan. The egg capsules senger 1979, Marthy 1987, Shigeno et al. 2001a,b, were transferred to the laboratory at the Department Shigeno & Yamamoto 2002, Kobayashi et al. 2013). of Biology, Chemistry and Marine Sciences in the Although some biochemical and immuno histo chem - University of the Ryukyus, as described in a previous ical studies have identified the main neuro transmitters study (Kobayashi et al. 2013). These egg capsules and neuromodulators present in the cephalopod brain were maintained in a 180 l circular polystyrene tank (Tansey 1979, Messenger 1996), little is known about consisting of a closed seawater system (OPEN-FIELD the neuronal mechanisms that underlie these complex tank, Aqua, 726 × 1065 × 303 mm, 60 l filtration tank behaviors in S. lessoniana. with a condenser and sterilizer). Hatchlings were iso- To reveal the functional network in the CNS that lated in a 20 l circular tank consisting of a closed sea- underlies brain functions linked to complex behaviors, water system (Multi-hydense® Aqua, 300 mm dia - we focused on one of the major neurotransmitters in meter, 180 l filtration tank) and reared for 100 to Kobayashi et al.: GAD immunoreactivity in the oval squid brain 99 112 d. The date on which the largest number of squid were rinsed 3 times with PB for 10 min, visualized us- hatched was defined as Day Zero. Water temperature ing the avidin-biotin-peroxidase complex (ABC) was maintained between 24.0 and 25.0°C throughout method, and counter-stained by he matoxylin. We dis- the experiment. Salinity was adjusted to approx. 35 criminated immunostaining and hema toxylin by the and pH was maintained above 7.8. Water quality and obtained colors—purple for hema toxylin and brown environmental factors were as follows: temperature for immunostaining. The specificity of the immunore- 24.1 to 24.7°C; salinity 34.0 to 36.5; pH 7.53 to 8.1 (pH action was checked by the antibody-absorption test was >7.8 during the majority of the experiment). using GAD antigen peptide (GAD, control peptide for Squid <14 d old were fed live prey (adult mysids AB1511, Millipore-Chemicon). Primary antibody was Neomysis japonica, guppy fry Poecilia reticulata, added to the antigen peptide (10 µg per m of diluted nauplii of brine shrimp Artemia salina). Squid >14 d antibody). No specific staining was obtained. old were fed frozen organisms (sakura shrimp Sergia lucens, anchovy Engraulis japonicus, common prawn Palaemon paucidens) 3 times per day. New hatch- Analysis lings were fed 4 times per day at approx. the same time each day. We measured the relative densities of GAD-posi- tive cell bodies in each lobe from light micrographs using Image J®, as previously reported (Bardou et Animals al. 2009). The density of GAD-positive fibers was de - termined by converting the intensity of gray in pho - Five young male Sepioteuthis lessoniana (100 to to graphs of sagittal sections into grayscale using 112 d old) reared in captivity were used in this study. Adobe Photoshop® CS. The dorsal mantle length and wet body weight of the squid were in the ranges of 61.2 to 93.1 mm and 32.5 to 53.6 g, respectively. According to criteria reported RESULTS by Segawa (1987), the stage of all animals used in this investigation was ‘young 2,’ and the shape of their General structure of oval squid CNS bodies was nearly identical to that of adults.
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