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338

GLOSSARY

Yakovlev, 1968) have maintained that the commissuration is preceded by the development of a massa commissuralis (q.v.), which implies some fusion of the medial hemispheric walls at the level of the hippocampal primordium.

Plate, cortical (Fig. 21-7): A neopallial feature first found in the embryo at stage 21 (Fig. 21-9). It consists of three to five rows of cells that have migrated radially from the ventricular layer and are arranged vertically. It increases in thickness and persists for long into the fetal period. Although formerly it was thought that only layers 2 to 5 develop from the cortical plate, it is now generally believed that layer 6 is also derived from the plate (Mrzijak et al., 1988). The migrating neurons that accumulate within the primordial plexiform layer are arranged in an outside–inside order. Synapses develop relatively late within the cortical plate, at about 23 weeks (Molliver et al., 1973), whereas they are already present in the primordial plexiform layer at stages 17–19.

Plate, neural (Fig. 8-2): The neural primordium that first becomes visible during stage 8 and is present in caudal areas up to stage 10. At the time of its first appearance it is slightly vaulted on each side of the neural groove. The prenotochordal part of the neural plate is the diencephalic region (neuromere D1 and the future rostral parencephalon). The epinotochordal portion of the neural plate (that overlying the notochord) develops a floor plate (q.v.).

Plate, optic: The median region that unites the optic primordia of the two sides (Fig. 10-3). It represents the rostral end of the neural plate, and it participates in the formation of neuromere D1.

Plate, prechordal: A multilayered accumulation of mesendodermal cells in close contact with the median part of the future prosencephalon in the human embryo (Figs. 8-3 and 8-6). The plate differs appreciably in the mouse and in the chick embryo. It has been unequivocally found first at stage 7, and is usually detectable at stage 8. The plate lacks a clearly visible, complete underlying sheet of endoderm. At stages 9 and 10 the plate is related to neuromere D1 (Muller¨ and O’Rahilly, 2003a).

Plates, alar and basal: See Laminae, alar and basal.

Plexuses, choroid: Intraventricular invaginations at stages 18–20 of choroidal (as distinct from ventricular) ependyma derived from the ventricular layer of the neural tube and characterized by tight junctions and tela choroidea (vascular pia mater). The plexuses are relatively very large in the embryo (Fig. 23-16). They produce cerebrospinal fluid (in contrast to the ependymal fluid of earlier stages) and probably a variety of growth factors.

Preplate: A term that is sometimes used (e.g., by Bystron et al., 2005) for the early marginal zone of the cortical primordium.

Prosomeres: The neuromeres of the prosencephalon.

Recess, isthmic (Fovea isthmi): The ventral limit of the mes-metencephalic sulcus (Fig. 17-5) (Bartelmez and Dekaban, 1962).

Recess, postoptic: The site where the optic sulci meet in the median plane (Fig. 10-3). This is the caudal limit of the chiasmatic plate.

Recess, preoptic: In later stages this depression indicates the rostral limit of the chiasmatic plate (Fig. 14-2).

Rhombomeres: The transverse swellings in the neural tube, known as neuromeres, are termed rhombomeres in the developing rhombencephalon, where they are clearly visible up to stage 17 (Muller¨ and O’Rahilly, 2003 b). They are originally four in number (Fig. 9-2C) and are termed A, B, C, and D. They increase in number by subdivision during stage 10 and are numbered 1, 2, 3 (from A), 4 (corresponding to B), 5, 6, 7 (from C), and 8 (corresponding to D and related to somites 1–4). Eight rhombomeres are generally identifiable from stage 11 to stage 17; in addition, the isthmus rhombencephali (q.v.) becomes apparent from stage 13 onwards. They are believed to result from transverse bands of high mitotic activity and they are maintained by cytoskeletal components, although their significance is still disputed. Cranial nerves 5 to 10 have a clear relationship to specific rhombomeres; the otic vesicle (Fig. 12-2 and 12-6), however, changes its position with regard to the rhombomeres, shifting from Rh.4 (in stage 10) to Rh.6 (in stages 14–17).

Roof plate: The plate consists of the dorsomedial cells of the neural tube (Fig. 21-7). It is believed to be induced by a morphogenic protein of ectodermal origin, and it may be important in causing differentiation of the dorsal part of the spinal cord.

Septum, prosencephalic: The septum verum (Andy and Stephan, 1968) is the basal part of the medial wall of the cerebral hemispheres. Hence it is formed at the time when the hemispheres expand beyond the lamina terminalis, beginning at stage 17. It is the area between the olfactory bulb and the commissural plate (Fig. 18- 2). The nuclei arising in it during the embryonic period are the medial septal nucleus, the caudal nucleus of the diagonal band, and the nucleus accumbens.

Sexual differentiation and brain development: All embryos are exposed to maternal estrogen, and male fetuses additionally to their own testosterone; the hypothalamus is especially involved. Later, these hormones play a “housekeeping” role in the growth and maintenance of cells of the brain in both sexes.


 

 

 

 

GLOSSARY

 

339

Situs neuroporicus (Fig. 12-7): The site of final closure of

the original components of the primordial plexiform

the rostral neuropore. It corresponds later to an area

layer are believed neither to decrease nor to disappear,

within the commissural plate (O’Rahilly and Muller,¨

but rather to undergo a significant and progressive di-

1989a, 2002).

 

 

 

lution (Mar´ın-Padilla, 1988a). The early subplate cells

Stalk,

hemispheric: The

original

connection

undergo regressive changes and they are progressively

replaced by new projection neurons (Mar´ın-Padilla,

(Streifenhugelstiel,¨

Hemispharenstiel:¨

His, 1904)

1988a).

 

 

between the diencephalon and the telencephalon,

 

 

 

 

 

which becomes a stalk from about stage 17. It becomes

Sulcus, hypothalamic (Table 20-1): An internal groove be-

greatly enlarged by fibers and tracts, especially by

tween the thalamus sensu lato (comprising the dorsal

the continuation of the internal capsule (Figs. 21-6,

and ventral thalami) and the hypothalamus sensu

22-10, and 22-11), namely the lateral prosencephalic

lato (comprising the subthalamus and hypothalamus

fasciculus (q.v.). See Sharp (1959) and Richter (1965).

sensu stricto). It begins and ends in the diencephalon

Stammbundel¨ : The term used by His for the fibers (lateral

(Fig. 17-4 inset).

 

prosencephalic fasciculus, q.v.) connecting the dorsal

Sulcus, intereminential: A term used by the present au-

thalamus and telencephalon and continuing also to

thors for the slight groove that appears at stage 18

the epithalamus and to the mesencephalon.

between the lateral and medial ventricular eminences

Stem cells, neural: The pluripotential stem cells of the

(Fig. 22-6A).

 

 

mammalian brain develop in the ventricular layer of

Sulcus limitans (Fig. 21-7 and 21-8): An internal groove

the embryo and fetus, as well as from the neural crest.

found bilaterally in the developing mesencephalon,

These cells develop into both neurons and glia. Neu-

rhombencephalon, and spinal cord. It is present at

ronal stem cells persist in the adult mammalian cen-

stage 12 and is the boundary between the alar and

tral nervous system (e.g., in the ependyma) and partic-

basal laminae (q.v.). In the human embryo the sul-

ipate in plasticity and regeneration, but they have the

cus limitans ends rostrally near the rostral end of the

immunocytochemical markers of glia. The only site

mesencephalon (Fig. 17-4). This point was long dis-

in the adult peripheral nervous system where produc-

puted in the past (Fig. 21-8). See also Laminae, alar and

tion of neural stem cells is documented is the olfactory

basal.

 

 

neuroepithelium. A pool of progenitor cells within the

 

 

Swellings, cerebellar: Bulges that are parts of the cere-

human dentate gyrus continues to produce new gran-

bellar plate, i.e., the alar lamina of the isthmic seg-

ule cells throughout life. Adult glial progenitors de-

ment together with that of rhombomere 1. The earlier

velop into oligodendrocytes and astrocytes (Comptson

appearing internal cerebellar swelling (innerer Klein-

et al., 1997). However, studies of embryonic and adult

hirnwulst of Hochstetter, 1929) is inside the fourth

stem cells still contain “red herrings” (Quesenberry

ventricle (Fig. 17-4). The external cerebellar swelling

et al., 2005) and much further work remains to be

(ausserer¨ Kleinhirnwulst) forms as an expansion at

done.

 

 

 

 

 

 

the site of the rhombic lip (Fig. 17-3). It is delimited

Subplate (Figs. 21-7 and 23-22): A derivative of the pri-

by a groove that corresponds to the later posterolat-

mordial plexiform layer (q.v.), which may participate

eral fissure of the cerebellum. The internal and ex-

in the specification of the cortical plate (q.v.). It has

ternal cerebellar swellings are sometimes referred to,

been termed a waiting compartment for incoming af-

respectively, as the intraventricular and extraventric-

ferent axons (Rakic). Catecholamine axons enter the

ular portions of the developing cerebellum.

 

telencephalic wall and occupy the subplate and (al-

 

Synencephalon (Fig. 13-8): The caudalmost part of the

though more sparsely) the marginal (subpial) layer

diencephalon, the portion that gives rise to the pre-

during the embryonic period (Verney et al. 2002). It

rubrum and the pretectum. It is delineated

ros-

is possible, therefore, that an initial contact between

trally by the habenulo-interpeduncular tract (fascicu-

catecholaminergic fibers and GABA-positive neurons

lus retroflexus) and caudally by the di-mesencephalic

is established early (Zecevic and Milosevic, 1997; Ver-

borderline passing between the two constituents of the

ney et al. 2002). However, several classes of afferent

posterior commissure.

 

fibers wait for weeks before penetrating the cortical

 

 

 

 

plate, and the role they play in the transitory synaptic

Telencephalon medium or impar: The first part of the te-

organization of the subplate is still unclear.

lencephalon to appear (at stage 10, Fig. 10-3) is lateral

 

A clear anatomical separation does not exist be-

in position. Only later (stage 14) do the lateral walls

tween the subplate and the intermediate layer; both

become domed and form the future cerebral hemi-

are characterized by an abundance of fibers (Figs. 23-

spheres (Muller¨

and O’Rahilly, 1985). The median part

21 and 23-22). The subplate gradually disappears dur-

of the telencephalon persists throughout life, so that

ing early infancy (Kostovic´ and Rakic, 1990). However,

a portion of the third ventricle remains telencephalic.


340

GLOSSARY

Torus hemisphericus: A ridge at the ventricular surface between the telencephalon and the diencephalon, and along which the cerebral hemispheres are evaginated (Fig. 14-2). An external di-telencephalic sulcus develops and accompanies it.

Torus opticus: See Plate, chiasmatic.

Velum transversum: A transverse ridge in the roof of the forebrain marking the limit between telencephalon and diencephalon (Fig. 14-2).

Ventricle, olfactory (Fig. 22-12): A prolongation of the lateral ventricle into the growing olfactory bulb at approximately stages 19 to 23, and also in the fetal period.

Ventricle, optic: At first (stage 13), the cavity of the optic vesicle, which is a prolongation of that of the diencephalon. Later it becomes the intraretinal slit between the external and internal strata of the optic cup, and ultimately the potential space (along which socalled detachment of the retina occurs) between layer 1 and layers 2–10 of the retina (Fig. 23-13).

Zona limitans intrathalamica: A zone that parallels the marginal ridge and sulcus medius between the dorsal and ventral thalami and is first recognizable as a thicker marginal layer at this site. Fibers of the zona are visible at stage 19 (Fig. 19-22). The zona is believed to form later the lamina medullaris externa. The marginal ridge, sulcus medius, and zona limitans intrathalamica are seen in Figure 21-14.

A P P E N D I X 1

CHANGING LENGTHS OF

THE BRAIN AND ITS

SUBDIVISIONS FROM

1

1

WEEKS

3 /2

TO 5 /2

(STAGES 9–16)

Figure A–1. (A) The actual lengths in mm, based on the authors’ studies of 25 embryos.

Stage

9

10

11

12

13

14

15

16

The Embryonic Human Brain: An Atlas of Developmental Stages, Third Edition. By O’Rahilly and Muller¨

Copyright C 2006 John Wiley & Sons, Inc.

341


342

1

1

WEEKS (STAGES 9–16)

A p p e n d i x 1 : CHANGING LENGTHS OF THE BRAIN AND ITS SUBDIVISIONS FROM 3 /2

TO 5 /2

Figure A–1. (B) Changes in length given as percentages of the total length of the brain, based on the authors’ studies of 91 embryos. The vertical rectangles in the rhombencephalon show the level of the otic primordia (Ot.) A-D, early (primary) neuromeres. 1-8, rhombomeres.

A P P E N D I X 2

COMPUTER RANKING

OF THE SEQUENCE OF

APPEARANCE OF

FEATURES OF THE BRAIN

Stage

7

8

9

 

10

11

12

13

14

15

Total

 

 

 

 

 

 

 

 

 

 

 

 

Total number

7

32

3

 

21

24

36

44

56

40

263

Good quality

7

21

3

 

12

18

22

20

36

26

165

Silver-treated

0

0

0

 

0

1

2

5

5

5

18

Greatest length (mm)

0.3−0.7 0.4−1.5 1.4±0.5 2.1±0.2 3.4±0.2 3.6±0.1 4.9±0.1 6.6±0.2 7.4±0.3

 

Age (weeks)

3

 

3

1

4

 

 

4 1

 

5

 

 

 

 

 

2

 

 

 

2

 

 

 

1. Neural groove

 

5/19

+

 

+

+

+

+

+

+

 

2. Otic disc/groove/pit

 

1/21

+

 

+

+

+

+

+

+

 

3. Neural groove closes

 

 

 

 

9/12

+

+

+

+

+

 

4. Optic sulcus

 

 

 

 

6/12

+

+

+

+

+

 

5. Optic vesicle

 

 

 

 

 

16/18

+

+

+

+

 

6. Entire notochord

 

 

 

 

 

5/18

17/17

+

+

+

 

7. Rostral neuropore closes

 

 

 

 

 

4/18

+

+

+

+

 

8. Otocyst

 

 

 

 

 

 

19/22

+

+

+

 

9. Adenohypophysial pocket

 

 

 

 

 

 

18/21

+

+

+

 

10. Ganglia of 5 and 7 are

 

 

 

 

 

 

15/19

+

+

+

 

compact

 

 

 

 

 

 

 

 

 

 

 

11. Rhombencephalic marginal

 

 

 

 

 

 

15/16

+

+

+

 

layer

 

 

 

 

 

 

 

 

 

 

 

12. Root of fourth ventricle is thin

 

 

 

 

 

1/18

16/19

+

+

+

 

13. Caudal neuropore closes

 

 

 

 

 

0/17

13/22

+

+

+

 

14. Hypoglossal roots appear

 

 

 

 

 

 

3/22

+

+

+

 

15. Lens disc

 

 

 

 

 

 

 

+

+

+

 

16. Intramedullary roots 5 and 7

 

 

 

 

 

 

 

13/13

35/35

+

 

17. Intramedullary roots 9–11

 

 

 

 

 

 

 

12/12

34/34

+

 

18. Nucleus of lateral

 

 

 

 

 

 

 

+

35/35

+

 

longitudinal fasciculus

 

 

 

 

 

 

 

 

 

 

 

19. Nucleus of 3

 

 

 

 

 

 

 

19/20

35/35

+

 

 

 

 

 

 

 

 

 

 

 

 

 

The Embryonic Human Brain: An Atlas of Developmental Stages, Third Edition. By O’Rahilly and Muller¨

Copyright C 2006 John Wiley & Sons, Inc.

343