Genoarchitectonic Profile of Developing Nuclear Groups in
the Chicken Pretectum
J.L. FERRAN, E. DUTRA DE OLIVEIRA, P. MERCHA
´
N, J.E. SANDOVAL, L. SA
´
NCHEZ-ARRONES,
M. MARTI
´
NEZ-DE-LA-TORRE, AND L. PUELLES
*
Department of Human Anatomy and Psychobiology, University of Murcia, and Centre for Biomedical Research on Rare Diseases
(CIBERER736), School of Medicine, Murcia, E30071, Spain
ABSTRACT
Earlier results on molecularly coded progenitor domains in
the chicken pretectum revealed an anteroposterior subdivi-
sion of the pretectum in precommissural (PcP), juxtacom-
missural (JcP), and commissural (CoP) histogenetic areas,
each specified differentially (Ferran et al. [2007] J Comp
Neurol 505:379 – 403). Here we examined the nuclei derived
from these areas with regard to characteristic gene expres-
sion patterns and gradual histogenesis (eventually, migra-
tion patterns). We sought a genoarchitectonic schema of
the avian pretectum within the prosomeric model of the
vertebrate forebrain (Puelles and Rubenstein [2003] Trends
Neurosci 26:469 – 476; Puelles et al. [2007] San Diego: Aca-
demic Press). Transcription-factor gene markers were used
to selectively map derivatives of the three pretectal histo-
genetic domains: Pax7 and Pax6 (CoP); FoxP1 and Six3
(JcP); and FoxP2, Ebf1, and Bhlhb4 (PcP). The combination
of this genoarchitectonic information with additional data
on Lim1, Tal2, and Nbea mRNA expression and other che-
moarchitectonic results allowed unambiguous character-
ization of some 30 pretectal nuclei. Apart from grouping
them as derivatives of the three early anteroposterior do-
mains, we also assigned them to postulated dorsoventral
subdomains (Ferran et al. [2007]). Several previously un-
known neuronal populations were detected, thus expanding
the list of pretectal structures, and we corrected some ap-
parently confused concepts in the earlier literature. The
composite gene expression map represents a substantial
advance in anatomical and embryological knowledge of the
avian pretectum. Many nuclear primordia can be recognized
long before the mature differentiated state of the pretectum
is achieved. This study provides fundamental notions for
ultimate scientific study of the specification and regional-
ization processes building up this brain area, both in birds
and other vertebrates. J. Comp. Neurol. 517:405– 451, 2009.
© 2009 Wiley-Liss, Inc.
Indexing terms: genoarchitectonics; pretectum; diencephalon; prosomeres; pretectal nuclei;
neuromeres; patterning; neurohistogenesis; neuronal migration
We still lack a widely accepted anatomical systematization
of the pretectum in vertebrates, probably because views on
this concept have greatly oscillated over time between the
conflicting columnar and segmental paradigms on the orga-
nization of the diencephalon (Puelles, 1995). Users of these
unreconcilable viewpoints employ different assumptions for
locating the mes-diencephalic and thalamo-pretectal bound-
aries, and their respective versions of the pretectum are
accordingly discrepant with regard to which neuronal com-
plexes, characterized as pretectal, as opposed to identifica-
tions as thalamic or mesencephalic formations (e.g., Kuhlen-
beck, 1973; Swanson, 1992; Altman and Bayer, 1995; Alvarez-
Bolado and Swanson, 1996; Redies et al., 2000; Puelles et al.,
2004, 2007).
The classic mes-diencephalic boundary concept was
heavily handicapped at the outset of brain developmental
studies by the unfortunate proposal by His (1893, 1895) of an
arbitrary oblique boundary plane, described by him as “a
tentative provisional reference,” which was traced between
the center of the posterior commissure and the mammillary or
retromammillary area. This border result is clearly unnatural in
the present era of molecular markers, since it falsely implies
that the longitudinal prerubral tegmentum is a tranversal mor-
phologic entity (Puelles, 1995; Puelles et al., 2004, 2007; Fer-
Grant sponsor: Spanish MEC; Grant number: BFU 2008-04156; Grant
sponsor: National Institutes of Health (NIH); Grant number: 1-R01-
MH070370-01A2; Grant sponsor: SENECA Foundation; Grant number:
04548/GERM/06 (no. 10891); Grant sponsor: CIBER de Enfermedades
Raras U736 (to L.P.); Grant sponsor: CIBERER postdoctoral researcher (to
J.L.F.); Grant sponsor: NIH; Grant number: 1-R01-MH070370-01A2 (post-
doctoral and predoctoral fellows to P.M., J.E.S.); Grant sponsor: FPI pre-
doctoral fellow of Spanish Ministry of Science (to L.S.A.).
*Correspondence to: Luis Puelles, Department of Human Anatomy and
Psychobiology, Faculty of Medicine, University of Murcia, 30100 Murcia,
Spain. E-mail: puelles@um.es
Received 23 January 2009; Revised 3 April 2009; Accepted 22 May 2009
DOI 10.1002/cne.22115
Published online June 11, 2009 in Wiley InterScience (www.interscience.wiley.
com).
The Journal of Comparative Neurology 517:405– 451 (2009)
Research in Systems Neuroscience
© 2009 Wiley-Liss, Inc.