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Adult neurogenesis in the brain of the Mozambique tilapia, Oreochromis mossambicus

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Abstract

Although the generation of new neurons in the adult nervous system (‘adult neurogenesis’) has been studied intensively in recent years, little is known about this phenomenon in non-mammalian vertebrates. Here, we examined the generation, migration, and differentiation of new neurons and glial cells in the Mozambique tilapia (Oreochromis mossambicus), a representative of one of the largest vertebrate taxonomic orders, the perciform fish. The vast majority of new cells in the brain are born in specific proliferation zones of the olfactory bulb; the dorsal and ventral telencephalon; the periventricular nucleus of the posterior tuberculum, optic tectum, and nucleus recessi lateralis of the diencephalon; and the valvula cerebelli, corpus cerebelli, and lobus caudalis of the cerebellum. As shown in the olfactory bulb and the lateral part of the valvula cerebelli, some of the young cells migrate from their site of origin to specific target areas. Labeling of mitotic cells with the thymidine analog 5-bromo-2′-deoxyuridine, combined with immunostaining against the neuron-specific marker protein Hu or against the astroglial marker glial fibrillary acidic protein demonstrated differentiation of the adult-born cells into both neurons and glia. Taken together, the present investigation supports the hypothesis that adult neurogenesis is an evolutionarily conserved vertebrate trait.

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Abbreviations

A:

Anterior thalamic nucleus

AC:

Anterior commissure

BO:

Olfactory bulb

BOgl :

Glomerular layer of the olfactory bulb

BOgra :

Granular layer of the olfactory bulb

bv:

Blood vessel

CC:

Crista cerebellaris

CCe:

Corpus cerebelli

CCegra :

Granular layer of corpus cerebelli

CCemol :

Molecular layer of corpus cerebelli

CE:

Central nucleus of the inferior lobe

ch:

Horizontal commissure

CM:

Corpus mamillare

CP:

Central posterior thalamic nucleus

Cven:

Ventral rhombencephalic commissure

D:

Dorsal telencephalon

DA:

Anterior part of the dorsal telencephalon

DC:

Dorsocentral telencephalon

DCa:

Anterior subdivision of the dorsal central telencephalon

DCad:

Dorsal part of the anterior subdivision of the dorsocentral telencephalon

DCm:

Medial subdivision of the dorsocentral telencephalon

DD:

Dorsal division of the dorsal telencephalon

DFl:

Nucleus diffusus lateralis of the inferior lobe

DFld:

Dorsal subdivision of nucleus diffusus lateralis of the inferior lobe

DFlv:

Ventral subdivision of nucleus diffusus lateralis of the inferior lobe

DFm:

Nucleus diffusus medialis of the inferior lobe

DL:

Dorsolateral telencephalon

DLa:

Anterior subdivision of the dorsolateral telencephalon

DLd:

Dorsal subdivision of the dosolateral telencephalon

DLp:

Posterior subdivision of the dorsolateral telencephalon

DLv:

Ventral subdivision of the dorsolateral telencephalon

DM:

Dorsomedial telencephalon

DMa:

Anterior subdivision of the dorsomedial telencephalon

DMdd:

Dorsal part of the dorsal subdivision of the dorsomedial telencephalon

DMdv:

Ventral part of the dorsal subdivision of the dorsomedial telencephalon

DMv:

Ventral subdivision of the dorsomedial telencephalon

DMvd:

Dorsal part of the ventral subdivision of the dorsomedial telencephalon

DMvv:

Ventral part of the ventral subdivision of the dorsomedial telencephalon

DP:

Dorsal posterior thalamic nucleus

Dp:

Posterior part of dorsal telencephalon

EG:

Eminentia granularis

G:

Glomerular nucleus

GC:

Central gray

H:

Habenula

Hv:

Ventral zone of the periventricular hypothalamus

IL:

Inferior lobe of the hypothalamus

ILdl:

Dorsolateral subdivision of the inferior lobe of the hypothalamus

ILvm:

Ventromedial subdivision of the inferior lobe of the hypothalamus

IPn:

Interpeduncular nucleus

LCe:

Lobus caudalis

LCegra :

Granular layer of the lobus caudalis

LH:

Lateral hypothalamic nucleus

LVII:

Lobus facialis

LX:

Lobus vagi

MLF:

Medial longitudinal fascicle

mol:

Molecular layer

nIII:

Nucleus oculomotorius

nRL:

Nucleus recessi lateralis

nRLl:

Lateral part of the nucleus recessi lateralis

nRLm:

Medial part of the nucleus recessi lateralis

nRP:

Nucleus recessi posterioris

nVd:

Descending trigeminal nucleus

nX:

Nucleus X (unidentified nucleus located between tOv and DFld)

P:

Preoptic region

PGm:

Medial part of the preglomerular nucleus

PP:

Periventricular preoptic nucleus

PPa:

Anterior part of the periventricular preoptic nucleus

PPm:

Medial part of the periventricular preoptic nucleus

PPp:

Posterior part of the periventricular preoptic nucleus

RL:

Recessus lateralis

RP:

Recessus posterioris

RV:

Rhombencephalic ventricle

Sc:

Suprachiasmatic nucleus

TA:

Nucleus anterior tuberis

TeO:

Optic tectum

TGN:

Tertiary gustatory nucleus

TGNl:

Lateral part of the tertiary gustatory nucleus

TGNm:

Medial part of the tertiary gustatory nucleus

TL:

Torus longitudinalis

TLA:

Torus lateralis

TLAi:

Inferior subdivision of the torus lateralis

tO:

Optic tract

tOd:

Tractus opticus dorsalis

tolfm:

Medial part of the olfactory tract

tOv:

Tractus opticus ventralis

TP:

Nucleus of the posterior tuberculum

TPP:

Periventricular nucleus of the posterior tuberculum

TS:

Torus semicircularis

tTB:

Tractus tecto-bulbaris

V:

Ventral telencephalon

v:

Ventricle

Val:

Lateral part of valvula cerebelli

Valgra :

Granular layer of the lateral part of valvula cerebelli

Valmol :

Molecular layer of the lateral part of the valvula cerebelli

Vam:

Medial part of valvula cerebelli

Vamgra :

Granular layer of the medial part of the valvula cerebelli

Vammol :

Molecular layer of the medial part of the valvula cerebelli

Vd:

Dorsal part of the ventral telencephalon

VLR:

Ventrolateral rhombencephalon

VM:

Ventromedial thalamic nucleus

Vs:

Supracommissural part of the ventral telencephalon

VVm:

Medial part of the ventral subdivision of the ventral telencephalon

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Acknowledgments

We thank Iulian Ilieş for helpful comments on a previous version of the manuscript. This study was funded by Tönjes-Vagt-Stiftung and Deutscher Akademischer Austauschdienst (to G.K.H.Z.); Gabinete de Relações Internacionais da Ciência e do Ensino Superior German-Portuguese exchange grant and Fundação Portuguesa para a Ciência e a Tecnologia research grant # PTDC/PSI/71811/2006 (to R.F.O.); and Ph.D.fellowship # SFRH/BD/44848/2008 (to M.C.T.). All experiments were carried out in accordance with the relevant law, the Deutsches Tierschutzgesetz of 1998.

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Authors and Affiliations

  1. Unidade de Investigação em Eco-Etologia, Instituto Superior de Psicologia Aplicada, Lisbon, Portugal

    Magda C. Teles & Rui F. Oliveira

  2. Champalimaud Neuroscience Programme, Instituto Gulbenkian de Ciência, Oeiras, Portugal

    Magda C. Teles & Rui F. Oliveira

  3. School of Engineering and Science, Jacobs University Bremen, Bremen, Germany

    Magda C. Teles, Ruxandra F. Sîrbulescu, Ursula M. Wellbrock & Günther K. H. Zupanc

  4. Department of Biology, Northeastern University, 360 Huntington Avenue, Boston, MA, 02115, USA

    Ruxandra F. Sîrbulescu & Günther K. H. Zupanc

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  1. Magda C. Teles
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Correspondence to Günther K. H. Zupanc.

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Teles, M.C., Sîrbulescu, R.F., Wellbrock, U.M. et al. Adult neurogenesis in the brain of the Mozambique tilapia, Oreochromis mossambicus . J Comp Physiol A 198, 427–449 (2012). https://doi.org/10.1007/s00359-012-0721-6

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