Distribution of choline acetyltransferase (ChAT) immunoreactivity in the central nervous system of a chondrostean, the siberian sturgeon (Acipenser baeri)

Abstract

All studies to date of cholinergic systems of bony fishes have been done in teleosts. To gain further insight into the evolution of the cholinergic systems of bony fishes, we have studied the brain of a chondrostean fish, the Siberian sturgeon (Acipenser baeri, Brandt), by using an antibody against choline acetyltransferase (ChAT). This study showed the presence of ChAT-immunoreactive (ChAT-ir) neurons in the preoptic region (parvocellular and magnocellular preoptic nuclei and suprachiasmatic nucleus), the periventricular and tuberal hypothalamus, the saccus vasculosus, the dorsal thalamus, and the habenula. The mesencephalic tegmentum contained ChAT-ir cells in the torus semicircularis and torus lateralis. The isthmus contained several cholinergic populations: the nucleus isthmi, the lateral nucleus of the valvula, the secondary visceral nucleus, and the dorsal tegmental nucleus. The motor neurons of the cranial nerves and the spinal motor column were strongly immunoreactive. The medial (sensory) trigeminal nucleus also contained a ChAT-ir neuronal population. The distribution of ChAT-ir neurons in the sturgeon brain showed some notable differences with that observed in teleosts, such as the absence of cholinergic cells in the telencephalon and the optic tectum. Several brain regions were richly innervated by ChAT-ir fibers, particularly the telencephalon, optic tectum, thalamus, posterior tubercle, and interpeduncular nucleus. The hypothalamo-hypophyseal tract, the tract of the saccus vasculosus, the fasciculus retroflexus, and an isthmo-mesencephalo-thalamic tract were the most conspicuous cholinergic bundles. Comparative analysis of these results suggests that teleosts have conserved most traits of the cholinergic system of the sturgeon, having acquired new cholinergic populations during evolution.

Organization of the cholinergic systems in the brain of two lungfishes, Protopterus dolloi and Neoceratodus forsteri

“…This feature has been reported in all amniotes studied (Houser et al 1983;Mesulam et al 1984;Satoh and Fibiger 1985;Vincent and Reiner 1987;Maley et al 1988;Sorenson et al 1989;Tago et al 1989;Medina et al 1993;Powers and Reiner 1993;Medina and Reiner 1994;St-Jacques et al 1996;Ichikawa et al 1997;Gravett et al 2009), as well as in all anamniotes studied (Marín et al 1997;Adrio et al 2000;Anadón et al 2000;Pérez et al 2000;Pombal et al 2001;González et al 2002a;Rodríguez-Moldes et al 2002;Mueller et al 2004;Giráldez-Perez et al 2009). This confirms the importance of the cholinergic nature in this part of the dorsal diencephalic conduction system, a highly conserved pathway that is likely a primitive feature for vertebrates (Bianco and Wilson 2009).…”

“…These large neurons are probably neurosecretory cells projecting to the neural lobe of the hypophysis, as has been observed in the magnocellular preoptic nucleus and some neurons of the hypothalamic tuberal nucleus in all anamniotes, from lampreys to amphibians (Marín et al 1997;Adrio et al 2000;Anadón et al 2000;Pérez et al 2000;Pombal et al 2001;González et al 2002a;Rodrí-guez-Moldes et al 2002;Mueller et al 2004). This feature is in contrast to the situation in amniotes, where cholinergic cells are absent from the neurosecretory nuclei in the preoptic region, although ChAT-ir cells have been described among or adjacent to the neurosecretory cells of the supraoptic nucleus (Mason et al 1983;Tago et al 1987;Medina et al 1993;Powers and Reiner 1993;Medina and Reiner 1994;Ichikawa et al 1997).…”

“…In general, no ChAT-ir cells have been seen in the striatum of fishes (Ekström 1987;Brantley and Bass 1988;Molist et al 1993;Adrio et al 2000;Anadón et al 2000;Pérez et al 2000;Mueller et al 2004;Giráldez-Perez et al 2009), the exception being those reported in lampreys, in the region homologous to the striatum (Pombal et al 1997(Pombal et al , 2001. In contrast, the presence of cholinergic cells in the striatum of amniotes is a very conservative feature (Marín et al 1998;Reiner et al 1998).…”

“…In other groups of fishes, cholinergic cells have been observed in the paraventricular nucleus of lampreys (Pombal et al 2001) and the tuberal hypothalamus of sharks, sturgeons and teleosts (Ekström 1987;Adrio et al 2000;Anadón et al 2000;Pérez et al 2000;Mueller et al 2004). In anurans and urodeles, ChATir cells were detected in the suprachiasmatic region (Marín et al 1997) and, additionally, in the infundibular hypothalamus in Xenopus laevis and in the gymnophionan Dermophis mexicanus (Marín et al 1997;González et al 2002a).…”

“…Furthermore, in teleosts cholinergic neurons in ventral telencephalic regions are considered to be homologous to the BFCS in tetrapods (Brantley and Bass 1988;Pérez et al 2000;Kaslin et al 2004;Mueller et al 2004) and, in particular, the cholinergic cells located in the lateral nucleus of area ventralis were compared to the nucleus basalis of Meynert (Mueller et al 2004). In contrast, in sturgeons, dogfishes and lampreys, the basal telencephalon is devoid of cholinergic neurons (Adrio et al 2000;Anadón et al 2000;Pombal et al 2001). Therefore, it was suggested that the ancestors of modern teleosts likely had a BFCS (Semba 2004) but, since only advanced teleosts have been examined for ChAT expression, and the status in the basal actinopterygians is unknown, it cannot be concluded that a BFCS first evolved in teleosts.…”