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Comparative analysis of the serotonergic systems in the CNS of two lungfishes, Protopterus dolloi and Neoceratodus forsteri

Abstract

The organization of the serotonergic system, one of the most important neurotransmitter 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. The present study is the first that provides a comprehensive and detailed map of the serotonergic structures in the brain of two representative species of lungfishes, the African lungfish (Protopterus dolloi) and the Australian lungfish (Neoceratodus forsteri), as revealed by immunohistochemistry against serotonin (5-HT). Lungfishes are currently considered the closest living relatives of tetrapods and represent an interesting group for the study of evolutionary traits in the transition from fishes to tetrapods. Distinct groups of serotonin immunoreactive cells were observed in the preoptic area, nucleus of the periventricular organ, pretectum, optic tectum and the long column of the raphe. Fiber labeling was widely distributed in all main brain subdivisions but was more abundant in regions such as the striatum, septum, amygdaloid complex, preoptic area, suprachiasmatic nucleus, lateral hypothalamic area, prethalamus, thalamus, mesencephalic tegmentum and rhombencephalic reticular formation. Comparison of these results with those from other classes of vertebrates highlights numerous common traits shared by most groups of fishes but also reveals that the serotonergic system in lungfishes largely resembles those of amphibians and other tetrapods.

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Abbreviations

a:

Cerebellar auricle

ac:

Anterior commissure

aol:

Octavolateral area

BST:

Bed nucleus of the stria terminalis

cCb:

Corpus cerebelli

Cbc:

Cerebellar commissure

cc:

Central canal

CeA:

Central amygdala

D:

Dorsal part of the thalamus

DCN:

Dorsal column nucleus

DF:

Dorsal funiculus

Dp:

Dorsal pallium

E:

Epiphysis

flm:

Fasciculus longitudinalis medialis

fr:

Fasciculus retroflexus

GCL:

Ganglion cell layer of the retina

gl:

Glomerular layer of the olfactory bulb

Hb:

Habenula

hc:

Habenular commissure

Hyp:

Hypophysis

igl:

Internal granular layer of the olfactory bulb

INL:

Inner nuclear layer of the retina

Ip:

Interpeduncular nucleus

IPL:

Inner plexiform layer of the retina

Ipn:

Interpeduncular neuropile

Is:

Isthmic nucleus

Jc:

Juxtacommissural pretectal nucleus

LA:

Lateral amygdala

Lc:

Locus coeruleus

LDT:

Laterodorsal tegmental nucleus

LF:

Lateral funiculus

lfb:

Lateral forebrain bundle

Lp:

Lateral pallium

Ls:

Lateral septum

M:

Median part of the thalamus

Ma:

Mammillary region

MC:

Mauthner cell

MCa:

Mauthner cell axon

MeA:

Medial amygdala

ml:

Mitral layer of the olfactory bulb

Mp:

Medial pallium

Mpd:

Dorsal part of the medial pallium

Mpv:

Ventral part of the medial pallium

Ms:

Medial septum

nVII:

Facial nerve

N.f:

Neoceratodus forsteri

nlla:

Anterior nerve of the lateral line

NPv:

Nucleus of the periventricular organ

nso:

Spino-occipital nerve

Nsol:

Nucleus of the solitary tract

nX:

Vagal nerve

ob:

Olfactory bulb

oc:

Optic chiasm

ONL:

Outer nuclear layer of the retina

OT:

Optic tectum

Pa:

Pallium

PA:

Pallidum

PC:

Purkinje cells of cerebellum

Pc:

Precommissural pretectal nucleus

P.d:

Protopterus dolloi

p 1–3:

Prosomeres 1–3

PO:

Preoptic area

PT:

Pretectum

PTh:

Prethalamus

r 0–8:

Rhombomeres 0–8

Rai:

Inferior raphe nucleus

Ram:

Median raphe nucleus

Ras:

Superior raphe nucleus

Ri:

Inferior reticular nucleus

RID:

Dorsal infundibular recesses

RIDi:

Inferior dorsal infundibular recesses

RM:

Retromammillary region

Rm:

Median reticular nucleus

Rs:

Superior reticular nucleus

S:

Septum

SC:

Suprachiasmatic nucleus

sco:

Subcommissural organ

sg:

Granular layer of the cerebellum

sgc:

Stratum griseum centrale of the mesencephalic tectum

sgp:

Stratum griseum periventriculare of the mesencephalic tectum

Smn:

Somatomotor neurons of spinal cord

sm:

Molecular layer of the cerebellum

sn:

Superficial nucleus

SN:

Substantia nigra

so:

Spino-occipital motor nucleus

sol:

Solitary tract

sop:

Stratum opticum of the mesencephalic tectum

SPa:

Subpallium

SPV:

Supraoptoparaventricular nucleus

Str:

Striatum

Tegm:

Tegmentum

Th:

Thalamus

Tor:

Torus semicircularis

TP:

Posterior tubercle

Tub:

Tuberal hypothalamus

V:

Ventral part of the thalamus

v:

Ventricle

VF:

Ventral funiculus

VP:

Ventral pallium

VTA/SN:

Ventral tegmental area/substantia nigra complex

III:

Oculomotor nucleus

IV:

Trochlear nucleus

Vm:

Trigeminal motor nucleus

VIIm:

Facial motor nucleus

IXm:

Glossopharyngeal motor nucleus

Xm:

Vagal motor nucleus

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Acknowledgments

We deeply thank Dr. Glenn R. Northcutt for providing the brains of Neoceratodus forsteri and for his continuous help and advise during many phases of the research. This research was supported by the Spanish Ministry of Science and Technology (Grant numbers: BFU2009-12315/BFI and BFU2012-31687).

Conflict of interest

The authors declare that they have no conflict of interest.

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Correspondence to Agustín González.

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López, J.M., González, A. Comparative analysis of the serotonergic systems in the CNS of two lungfishes, Protopterus dolloi and Neoceratodus forsteri . Brain Struct Funct 220, 385–405 (2015). https://doi.org/10.1007/s00429-013-0661-0

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Keywords

  • Serotonin
  • Immunohistochemistry
  • Hypothalamus
  • Raphe
  • Lungfish
  • Brain evolution