The Brain of the Archerfish Toxotes chatareus: A Nissl-Based Neuroanatomical Atlas and Catecholaminergic/Cholinergic Systems

Abstract

Over recent years, the seven-spot archerfish (Toxotes chatareus) has emerged as a new model for studies in visual and behavioral neuroscience thanks to its unique hunting strategy. Its natural ability to spit at insects outside of water can be used in the laboratory for well controlled behavioral experiments where the fish is trained to aim at targets on a screen. The need for a documentation of the neuroanatomy of this animal became critical as more research groups use it as a model. Here we present an atlas of adult T. chatareus specimens caught in the wild in South East Asia. The atlas shows representative sections of the brain and specific structures revealed by a classic Nissl staining as well as corresponding schematic drawings. Additional immunostainings for catecholaminergic and cholinergic systems were conducted to corroborate the identification of certain nuclei and the data of a whole brain scanner is available online. We describe the general features of the archerfish brain as well as its specificities, especially for the visual system and compare the neuroanatomy of the archerfish with other teleosts. This atlas of the archerfish brain shows all levels of the neuraxis and intends to provide a solid basis for further neuroscientific research on T. chatareus, in particular electrophysiological studies.

Organization of the catecholaminergic systems in two basal actinopterygian fishes, Polypterus senegalus and Erpetoichthys calabaricus (Actinopterygii: Cladistia)

“…Cells in Vd–Vn are probably the source of the pallial innervation (Holmes & Northcutt, ), although the posterior tubercle and the locus coeruleus may be other sources of pallial catecholaminergic innervation (Northcutt, ). The presence of TH+/DA+ cells in the subpallium (obviating the TH‐ir cells of preoptic area, see below) is a primitive feature described in agnathans, chondrichthyes and all actinopterygian fishes (Karoubi et al, ; Yamamoto et al, ), whereas these cells are generally absent in sarcopterygian vertebrates with the exception of TH‐ir cells reported in the striatum of monotremes and primates (Betarbet et al, ; Manger et al, ), and mice, which express TH mRNA in neurons of the striatum and amygdala during development and are persistent in adulthood (Baker et al, ; Bupesh et al, ; Marín et al, ). In turn, dense TH‐ir innervation is observed in the basal ganglia and septum of all sarcopterygians that was related to the development of the dopaminergic cell population in the mesencephalic tegmentum (López & González, ; Reiner, ).…”

“…This region is characterized by the presence of the magnocellular nucleus that forms the neurosecretory hypothalamo‐hypophyseal system (Nieuwenhuys, ). Only in teleosts, dopaminergic cells have been reported in the “preoptic” magnocellular nucleus (Bhat & Ganesh, ; Karoubi et al, ; Yamamoto et al, ). Also within the paraventricular region, CSF‐contacting cells in the organum vasculosum of some teleosts, lungfishes, and urodele amphibians contain dopamine (Corio, Thibault, & Peute, ; López & González, ; Morona & González, ; Mukuda et al, ).…”

“…In the alar plate of the rostral diencephalic segment (p3) of cladistians, a group of dopaminergic cells is located in the prethalamus. This prethalamic group is equivalent to the TH‐ir/DA‐ir cells located in the ventral thalamic area of elasmobranchs, chondrosteans, and teleosts (Adrio et al, ; Karoubi et al, ; Sas et al, ; Yamamoto et al, ). In addition, they are readily comparable to the dopaminergic cells in the zona incerta of mammals (the A13 group) and other amniotes (Smeets & González, ), and to the named periventricular zona incerta nucleus of amphibians and lungfishes (López & González, ; Milán & Puelles, ).…”

Organization of the catecholaminergic systems in the brain of lungfishes, the closest living relatives of terrestrial vertebrates

“…This conspicuous innervation resembles more the situation of amniotes than that of anamniotes (see Reiner, ) and it can be easily related to the development of important DA cell groups in the mesencephalic tegmentum (see below). Differently from the pallium, no TH‐ir cells are observed in the subpallium of lungfishes, in strict contrast with agnathan, chondrichthyans, and actinopterygian fishes (Northcutt et al, ; Yamamoto et al, ; Karoubi et al, ) that possess significant DA cell populations in homolog regions to the basal ganglia of sarcopterygians (González et al, ). Results in mice have shown the presence of TH mRNA and protein expressing cells in the striatum and other parts of the subpallium during development, which are persistent in adulthood although they are less numerous, generally show weak mRNA expression, and some appear to lack the protein (Bupesh, Vicario, Abellán, Desfilis, & Medina, ).…”

“…Numerous studies of the CA systems have been conducted in most fish groups (Kaslin & Panula, ; Rink & Wullimann, ,; O'Connell & Hofmann, ; Tay, Ronneberger, Ryu, Nitschke, & Driever, ; Yamamoto, Ruuskanen, Wullimann, & Vernier, ; Carrera, Anadón, & Rodríguez‐Moldes, ; Schweitzer, Lohr, Filippi, & Driever, ; Goodson & Kingsbury, ; Karoubi, Segev, & Wullimann, ; for older literature see cites in these articles), but they have been especially underexplored in the brain of lungfishes (Reiner & Northcutt, ; Bruzzone, d'Amora, Angelini, & Vallarino, ; González & Northcutt, ). The aim of the present study was to analyze in detail the anatomy of the CA system in the brain of one African lungfish, P. dolloi , and the Australian lungfish, N. forsteri , as representatives of the two extant orders of lungfishes.…”