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Spatiotemporal expression patterns of Pax6 in the brain of embryonic, newborn, and adult mice

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Abstract

The transcription factor Pax6 has been reported to specify neural progenitor cell fates during development and maintain neuronal commitments in the adult. The spatiotemporal patterns of Pax6 expression were examined in sagittal and horizontal sections of the embryonic, postnatal, and adult brains using immunohistochemistry and double immunolabeling. The proportion of Pax6-immunopositive cells in various parts of the adult brain was estimated using the isotropic fractionator methodology. It was shown that at embryonic day 11 (E11) Pax6 was robustly expressed in the proliferative neuroepithelia of the ventricular zone in the forebrain and hindbrain, and in the floor and the mesencephalic reticular formation (mRt) in the midbrain. At E12, its expression emerged in the nucleus of the lateral lemniscus in the rhombencephalon and disappeared from the floor of the midbrain. As neurodevelopment proceeds, the expression pattern of Pax6 changes from the mitotic germinal zone in the ventricular zone to become extensively distributed in cell groups in the forebrain and hindbrain, and the expression persisted in the mRt. The majority of Pax6-positive cell groups were maintained until adult life, but the intensity of Pax6 expression became much weaker. Pax6 expression was maintained in the mitotic subventricular zone in the adult brain, but not in the germinal region dentate gyrus in the adult hippocampus. There was no obvious colocalization of Pax6 and NeuN during embryonic development, suggesting Pax6 is found primarily in developing progenitor cells. In the adult brain, however, Pax6 maintains neuronal features of some subtypes of neurons, as indicated by 97.1% of Pax6-positive cells co-expressing NeuN in the cerebellum, 40.7% in the olfactory bulb, 38.3% in the cerebrum, and 73.9% in the remaining brain except the hippocampus. Differentiated tyrosine hydroxylase (TH) neurons were observed in the floor of the E11 midbrain where Pax6 was also expressed, but no obvious colocaliztion of TH and Pax6 was detected. No Pax6 expression was observed in TH-expressing areas in the midbrain at E12, E14, and postnatal day 1. These results support the notion that Pax6 plays pivotal roles in specifying neural progenitor cell commitments and maintaining certain mature neuronal fates.

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Abbreviations

3V:

Third ventricle

4V:

Fourth ventricle

5PC:

Motor trigeminal nucleus, parvicellular part

AA:

Anterior amygdaloid area

Amg:

Amygdala

AO:

Anterior olfactory nucleus

AOP:

Anterior olfactory area posterior part

APT:

Anterior pretectal nucleus

BL:

Basolateral amygdaloid nucleus

BM:

Basomedial amygdaloid nucleus

Cb:

Cerebellum

Ce:

Central amygdaloid nucleus

Ceph:

Cephalic flexure

CG:

Central gray

Cx:

Cortex

DC:

Dorsal cochlear nucleus

DG:

Dentate gyrus

Dien:

Diencephalon

DLL:

Dorsal nucleus of the lateral lemniscus

DR:

Dorsal raphe nucleus

DTg:

Dorsal tegmental nucleus

DTT:

Dorsal tenia tecta

ECu:

External cuneate nucleus

EGL:

External granular layer of developing cerebellum

EP:

Entopeduncular nucleus

E/OV:

Ependymal and subendymal layer/olfactory ventricle

F:

Nucleus of the fields of Forel

FovIs:

Fovea isthmus

Gi:

Gigantocellular reticular nucleus

Gl:

Glomerular layer of the olfactory bulb

GP:

Globus pallidus

GrC:

Granule cell layer of cochlear nuclei

HDB:

Nucleus of the horizontal limb of the diagonal band

I:

Intercalated nuclei of the amygdala

IEn:

Intermediate endopiriform nucleus

InC:

Interstitial nucleus of Cajal

IO:

Inferior olivary nucleus

Is:

Isthmus

isRt:

isthmic reticular formation

JPLH:

Juxtaparaventricular part of lateral hypothalamus

La:

Lateral amygdaloid nucleus

LC:

Locus coeruleus

LD:

Laterodorsal thalamic nucleus

LDTg:

Laterodorsal tegmental nucleus

LHb:

Lateral habenular nucleus

Li:

Linear nucleus

LL:

Nucleus of the lateral lemniscus

LP:

Lateral posterior thalamic nucleus

LPO:

Lateral preoptic area

LRt:

Lateral reticular nucleus

LSI:

Lateral septal nucleus, intermediate part

LV:

Lateral ventricle

MCPC:

Magnocellular nucleus of the posterior commissure

Me:

Medial amygdaloid nucleus

Mesen:

Mesencephalon

MHb:

Medial habenular nucleus

MnR:

Median raphe nucleus

mRt:

mesencephalic reticular formation

MS:

Medial septal nucleus

MVe:

Medial vestibular nucleus

MVPO:

Medioventral periolivary nucleus

PAG:

Periaqueductal gray

PaXi:

Paraxiphoid nucleus of thalamus

Pc:

Posterior commissure

PCom:

Nucleus of the posterior commissure

PDTg:

Posterodorsal tegmental nucleus

Pir:

Piriform cortex

PL:

Paralemniscal nucleus

PLH:

Peduncular part of lateral hypothalamus

Pn:

Pontine nuclei

PrC:

Precommissural nucleus

PrG:

Pregeniculate nucleus

PrTh:

Prethalamus (prosomere 3)

PrThE:

Prethalamic eminence

Ptec:

Pretectum

Rhomb:

Rhombencephalon

Rt:

Reticular thalamic nucleus

RtTg:

Reticulotegmental nucleus of the pons

SN:

Substantia nigra

SPFPC:

Subparafascicular thalamic nucleus, parvicellular part

SubG:

Subgeniculate nucleus

SuVe:

Superior vestibular nucleus

Telen:

Telencephalon

Tu:

Olfactory tubercle

VC:

Ventral cochlear nucleus

VCA:

Ventral cochlear nucleus, anterior part

VDB:

Nucleus of the vertical limb of the diagonal band

VEn:

Ventral endopiriform claustrum

VP:

Ventral pallidum

VTT:

Ventral tenia tecta

VTA:

Ventral tegmental area

VZ:

Ventricular zone

X:

Nucleus X

ZI:

Zona incerta

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Acknowledgments

We thank Dr. Huazheng Liang, Dr. Emma Schofield, and Mr Hua Zhao for technical support. This work was supported by the Christopher and Dana Reeve Foundation and an Australia Fellowship awarded to Professor George Paxinos by the National Health and Medical Research Council (NHMRC) (466028).

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Authors and Affiliations

  1. Neuroscience Research Australia, Randwick, Sydney, NSW, 2031, Australia

    Deyi Duan, Yuhong Fu, George Paxinos & Charles Watson

  2. School of Medical Science, University of New South Wales, Sydney, NSW, 2052, Australia

    George Paxinos

  3. Faculty of Health Sciences, Curtin University, Shenton Park Health Research Campus, GPO Box U1987, Perth, WA, 6845, Australia

    Charles Watson

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  1. Deyi Duan
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  2. Yuhong Fu
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  3. George Paxinos
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Correspondence to Charles Watson.

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Duan, D., Fu, Y., Paxinos, G. et al. Spatiotemporal expression patterns of Pax6 in the brain of embryonic, newborn, and adult mice. Brain Struct Funct 218, 353–372 (2013). https://doi.org/10.1007/s00429-012-0397-2

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  • DOI: https://doi.org/10.1007/s00429-012-0397-2

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