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

Abstract

Lungfishes (dipnoans) are currently considered the closest living relatives of tetrapods. The organization of the cholinergic systems in the brain has been carefully analyzed in most vertebrate groups, and major shared characteristics have been described, although traits particular to each vertebrate class have also been found. In the present study, we provide the first detailed information on the distribution of cholinergic cell bodies and fibers in the central nervous system in two representative species of lungfishes, the African lungfish (Protopterus dolloi) and the Australian lungfish (Neoceratodus forsteri), as revealed by immunohistochemistry against the enzyme choline acetyltransferase (ChAT). Distinct groups of ChAT immunoreactive (ChAT-ir) cells were observed in the basal telencephalon, habenula, isthmic nucleus, laterodorsal tegmental nucleus, cranial nerve motor nuclei, and the motor column of the spinal cord, and these groups seem to be highly conserved among vertebrates. In lungfishes, the presence of a cholinergic cell group in the thalamus and the absence of ChAT-ir cells in the tectum are variable traits, unique to this group and appearing several times during evolution. Other characters were observed exclusively in Neoceratodus, such as the presence of cholinergic cells in the suprachiasmatic nucleus, the pretectal region and the superior raphe nucleus. Cholinergic fibers were found in the medial pallium, basal telencephalon, thalamus and prethalamus, optic tectum and interpeduncular nucleus. Comparison of these results with those from other classes of vertebrates, including a segmental analysis to correlate cell populations, reveals that the cholinergic systems in lungfishes largely resemble those of amphibians and other tetrapods.

Comparative Analysis of the Organization of the Cholinergic System in the Brains of Two Holostean Fishes, the Florida Gar <b><i>Lepisosteus platyrhincus</i></b> and the Bowfin <b><i>Amia calva</i></b>

“…These experiments were added because the neuroanatomy of holosteans is not well documented, and the combined localization of ChAT-ir structures and TH-ir, CB-ir and CR-ir structures was useful in clarifying the actual position of certain cell groups, as proved in our previous studies [López et al, 2012.…”

“…Virtually all cholinergic groups first described and classified in the brains of rats [Mesulam et 112 al., 1983a] and macaque monkeys have been subsequently identified in all tetrapods. Moreover, in a recent study of the organization of the cholinergic systems in the brain of two lungfishes, the closest living relatives of tetrapods, the common organization with tetrapods was particularly evident [López et al, 2012].…”

“…Therefore, the main goal of the present study was to provide the first detailed information on the localization of cholinergic cell bodies and fibers in the brain of two representative species of holosteans, the Florida gar Lepisosteus platyrhincus and the bowfin A. calva . To facilitate comparisons, we used the same methods as in former studies [López et al, 2012, and we also compared our results with data from other vertebrate classes to shed light on the evolution of the cholinergic system and extend what is known about this neurotransmitter system. In addition, we combined the Cladogram showing the relationships of the four major groups of vertebrates: agnathans, cartilaginous fishes, ray-finned fishes and the sarcopterygian radiation of lobefinned fishes.…”

Cholinergic left-right asymmetry in the habenulo-interpeduncular pathway

“…The mHb-IPN tract is a major cholinergic system across vertebrates (6)(7)(8)(9)(10)(11); however, it is still unresolved whether this pathway is cholinergic in zebrafish. Cholinergic neurons are defined by the presence of choline acetyltransferase (ChAT), which synthesizes ACh from choline and acetyl CoA, and vesicular acetylcholine transporter (VAChT), which packages ACh into synaptic vesicles.…”

The Relationship between Branchiosomatic and Pulmosomatic Indices in the African Lungfish, Protopterus Annectens of Anambra River, Nigeria

“…In the Australian lungfish, Neoceratodus forsteri, all oxygen uptake while at rest are obtained in the aquatic exchange via the gills. (Lenfant et al, 1966;Joss, 2011) The single or unpaired lung in N. forsteri just serves as an accessory respiratory organ during increased physical stress or in highly polluted waters that kill other fishes (Grigg, 1965;Joss, 2011;Lopez et al, 2012).…”