ATLAS Steven B. Oppenheimer Richard L. C. Chao
a '. ~
....-< Atlas of Embryonic Development
Stevp.n K. Oppenheimer Richard L. C. Chao
Califomia Stale 1.ll1ivpr~ily, Northridge Copyright C 1984 byAllyn and Bacon, Inc., 7Well5 Avenue, Newton, Mas5achusetts 02159. All rights reserved. No part of the material protected by this COfliright BOIice may be reproduce:! or util1~ed in any form orbyany means, electronic or mecltanical, inc1udi ngph-otocopying.. recording. orbyany information storage and retrieval system, without written permission from the copyright owner.
library of Congress UtaJosiI1l in Publication Data
Oppenheimer, 5te"l'e!1 8~ 1944- Moils of embryonic development 1. Embryology--Atlases.1. Chao, Richard L. C. U. Title. [DNLM: 1. Embryology-Atlases. Q5 617062a] QL956.065a 1984 597.6'0413 83-27152 ISBN 0-205-{)6099-5
Printed in the United State5 01 America.
10987654321 88 87 86 8S 84 Preface Spermatogenesis and Oogenesis 1 I The Frog 5 A Frog Gametes 11 B Frog Blastula and Gastrula 14 C Frog Neurula 19 D Frog Tailbud, 4 mm Stage 29 E Frog, 5-8 mm Stages 36 F Frog, 10-18 mm Stages 45 II The Chick 55 A Chick Gastrula 58 B Ch ick, 26-33 Hour Embryos 61 C Chick, 50 Hour Emblyo 75 D Chick, 3-4 Day Embryos 86 III The Mammal 105 A Cat and Rat Gonads 107 B Pig, 6 mm Embryo 11 0 C Pig, 10 mm Embryo 113 o Human Development 132 Appendix 135 Pla nes and Sections Term inology Used in this Atlas 136 Obtai ni ng Frog Embryos for Microscopy for this Atlas 137 Obtaining Chick Embryos for Microscopy for this Atlas 138 Preparation of Specimens for Scann ing Electron Microsco py (or this Atla s 139 Refere nces Used for Preparing Embryos for Scanning Electron Microscopy 140 Light Microscopy Eq uipment Used for this Atlas 141 Holtfreter's Solution 142 Amphi bian Ringer's Solution 143 Howard Ringer's Solution 144 Glossary 145 Preface
Th is alla$ includes light micrographs and scanning electron micrographs of sped mens used in most developmental biology and embryology courses. We include the Kanning micrographs to shOlvthree-dimensiOllal qualities such as texture and depth that wou ld not be apparent from light micrographs alone. All fjgures are labeled for easy study, and transver>e ~1iom inciLIle diagrams that indicate the position of the section in the whole embryo. Developmental timetables and sketches incl uded should help ,Iudents under stand the sequence of e\en ~ occurring during embryonic development from a strlJctural standpoint. tn addition, drawings have been placed in appropriate sections of this atlas that wil l help students grasp the nature of the tissue movements and rearrangements that lead to the observed strLCtural changes that are characteristic of different devekpmental stages. Finally, a glossary of terms is included that will faci litate the definition of structures labeled in the micrograph ,. We thank Mary Beth Finch, Jim Sm ith, Joh n Gi lman, Vicky Prescott and Sandi Kirshner for excellent assistance in the development and production of this Ixx:.>k and the entire staff of Allyn and Bacon for concerted effort;; in the final stages of its prod; ction and distribution. Spermatogenesis and Oogenesis
prophiSe of mei o,;. J
leptotene
I p.chyten. I ~ d,plot.n~
~ :.105" miY be arrested in diplotene for many month, or yurs (for example, ~ meuph= __' an. phue 12 to SO yeirs in hum. n beiniS)
secondiry ooc;yte
Figure 1. Meiosis I in vertebrate oogenesis. From S. B. Oppenheimer, Introduc tion to Embryonic Development, 2nd Ed. (BostOll : Allyn and Bacon, 1984). -- ~-- I J.
. -_• I I
~-_1..._, _.""- _ 'ot ___ 1 II ""'-- . I I -. SPERMATOGENESIS AND OOGENESIS J
spermatogonia'"
Figure J. Summary of spermatogenesis. From S. B. Oppenheimer, IntJoduction to Embryonic Development, 2nd Ed . (Boston: Allyn and Bacon, 1984). 4 SPERMATOGEN ESIS AN O OOGENESIS
oocyle 1\ m""' AA ,, o 0
SP ERM ATOG ENES IS OOGENES IS
Figure 4. Comparison of spermatogenesis and oogenesis. From S. B. Oppen heimer, Introducrion to Embryonic Dcvelopmcnt, 2n d Ed . (Boston: Allyn an d Bacon, 1984). I Th Fro THE FROG 7
TABLE 1. Development of Rana pipiens at la"c
Stage Age in Size in number hours millimeters Characteristic s
0 1. 75 unfertilized egg 2 1. 0 1.8 gray crescent 3 3.5 1. 8 2 cell s 4 4.5 1. 8 4 cells 5 5. 7 1. 8 8 cells 6 6.5 18 16 ce ll s 7 7.5 1.8 32 cells 8 16 1.8 early blastula 9 21 1.8 late blastula 10 26 1.8 early gastrula (dorsal li p) 11 34 1. 9 middle ga strula (crescent blastopore) 12 42 2.0 late gastrula (yo lk plug) 13 50 2.2 neural pl ate 14 62 2.3 neu ral fo lds 15 67 2.4 cil ia rotation begins 16 72 2.5 complete neural tube 17 84 3. 0 tai l bud 18 96 4.0 muscular movement 19 11 8 5.0 heart beats 20 140 6.0 gil) ci rcu lation and hatching 21 162 7.0 mouth open; cornea is transparent 22 192 8.0 tail fi n circulati on 23 216 9.0 opercular fo ld; teeth 24 240 10.0 operCU lu m closed on righ t 25 284 11. 0 operculum complete
IBa sed on results of W. Shumway, Anal. Rec. 78: 139-148 (1940)) 8 THE FROG
fert ilized
••cleav ,1e.ge
" ta ilbud
~ ~ ~ I I
'i]~ ) d ~. gill bud, y" V
" ~ , '" ,1 V 11 , I I , , ]
\' " d V' hatching. gill circuld!inn
} "~ll ,I ~~: ,! , , r' e" ', , ... ' : J ! \ r } \0;' , 1"
moulh orx' ~
Tab le 1. Stages of frog deve lopment (continurdi. d, View from Jl1imal po le (frontal view); c, CJlldJI (b l asto~ r JIJ vi ew; d, dOrs.ll view; >, left la tera l view; v, ventral view. {From Del'e!opment of the Vert r br
___ tailfin circulation
opercula r foId_
d
--- right operculum cI <»ed
operculum complete _
. .; ." -. :;f" 1 ___ metamorpho,i. ~, .-.. ,;
Table 1. Stages of frog development (continued) . .a, View from an imal pole (frontal view); c, caudal (blastoporal) view; d, dorsal view; 5, left lateral view; II, ventra l view. (From Development of the Vertebrates by Emil Witschi. Copyright 1956 by W. B. Saunders Co. Used with permission of the W. B. Saunders Co.) 10 THE FROG
d
d
metamorphosis
Table 1. Stages of frog development (continued) . il, View from animal pole (frontal view); c, caudal (blastoporal) view; d, dorsal view; s, left lateral view; v, ventral view. (From Development of the Vertebrates by Emil Witschi. Copyright 1956 by W. B. Saunders Co. Used with permission of the W. 13. Saunders Co.) A. Frog Gametes
nucleoli (black dots)
theca externa
nuclear membrane
oocyte
oocyte nucleus (ge rm inal vesicle)
shrinkage artifact
Figure 5. Frog ovary. (66,6 x)
11 12 THE FROG
nuclei of nuclear follicle cells oocyte cytoplasm membrane
nucleoli nucleus (germinal vesicle)
Figure 6. Frog oocyte, enlarged. (621.6x) A. Frog Gametes 13
seminiferous tubules
spermatocytes sperm lumen Sertoli cell
Figure 7. Frog testis s~owing seminiferous tubule. (404.8x ) B. Frog Blastula and Gastrula
anima l region blastocoel
artifacts figure 8. Early frog blastu la. scanning electron micrograph. (137.2 x ) B. Frog Blastula and Gastrula 15
micromeres an ima) (dark spots are nuclei) pole fe rti lization membrane
blastocoel
shrinkage artifact macromeres vegetal pole figure 9. Frog blastula. (92.5 xl 16 THE FROG
neur~ltube
epidermis
•
lip
nQll-ootcx:hord~1 dOfS.Illip mesoderm be,in ning , , archenteron ,-"'m~."';; .. neur.1 plue epidermi, endoderm ~;<7 n,ural tuhe \'O;;;':!C->\\p'O.Pe<;tive ~rch en l . ron' notochord rr----.;
r' ,.-: ' '--,-c' . Pro.~ti~ e' prospective . . . ' A _A • nOll'nQlcx:hord~1, i",~ , :,::::,"~"~_:::::":m:,:'~ mesoderm prospective , 1 notcx:hord - ::~::;,;~~. epidermis "I ,.J
Figure to. Gastrulation in the amphibian. Keller and colleagues, working with Xenopus, a frog, found that prospective mesoderm may be located in deeper layers of the blastula instead of in surface regions. After W. Vogt., Raux Arch. 120, 385-706 (1929). From S. B. Oppenheimer, introduction to Embryonic De velopment 2nd Ed. (Boston; Allyn and Bacon, 1980). B. Frog Blastula and Ga<;trula 17
fertilization membrane blastocoel
blastopore dorsal lip of blastopore
Figure 11 . Early frog gostrulo. (92 S x ) 18 THE FROG
archenteron roof archenteron
dorsa! lip of blastopore
yo lk plug ventral lip of blastopore
fert il ization membrane
Figure 12. Frog yolk plug. (97.5 x ) C. Frog Neurula
non-notochordal mesoderm o
(I.) tWO layered st.n . : oule, Ibl 1,1 ectoderm and inner mesendode,m neuf.ltu!>c
notochord
somite intermediate me.o endoderm Id) Figure 13. Formation of the three-layered state in the amphibian. Coelom for mation occurs by mesodermal splitting. From S. 8. Oppenheimer, Introduction to Embryonic Development, 2nd Ed. (Boston: Allyn and Bacon, 1984). 20 THE FROG neural folds prospective epidermis foregut yolky endoderm fertilization membrane Figure 14. Frog embryo, neural fold stage, transverse section through foregut. (185 xl C. Frog Neurul a 21 neural groove neural fold fertilization membrane somite (epimere) notochord hypomere prospective epidermis yolky endoderm Figure 15. Frog embryo, neural fold stage, transverse section through midgut. (185 x) 22 THE FROG fertilization membrane neural groove neural fold prospective epidermis Figure 16. Frog embryo, neural fold stage, transverse 5ection through hindgut. (185 x) C Frog Neuru la 23 epidermi, mesoderm n"rvou, layer epiderm" is n<'u renteric canal do".1 projection of hindgut CIOlinS bla,topore ve nlfal diverticulum 01 hioo gul diverticulum venlral diverticulum mesenchyme livc r d i"erticulum D. 01 hioogul Figure 17. Beginning neurJI fold siage of frog emhryo from prepared material. (A) Begin ni ng neural fold slagc as seen from dorsal view. (B) Sagiu,ll $Celion near median plane of embryo similar 10 thai ,hown in (A). (CJ Same as (B), showing organ-forming areas. (D) Midsaginal sect ion of cauda l end of frog em bryo. Observe that the blastopore practiCJlly is closed, while the dorsal divertic ulum of the hindgut connects with the neurocoel to form the neurenteric canal. Observe, also, ventral diverticu lum of hindgut. From O. E. Nelsen, Comparative Embryology of !he VCr!ebr,lles (New York: McGraw-Hili, 1953). 24 THE FROG brain (neural tube) mesoderm , epidermis endoderm pharynx L figure 18. Frog embryo, neural tube stage, transverse section through fo regut. (185 X) - C Frog Neurula 25 rhombencephalon (neural tube) notochord epidermis foregut yolky endoderm Figure 19. Frog embryo, neura l tube stage, tran sve rse sec tion through foregut. (106 x) 26 THE FROG spinal cord (neural tube) mesoderm midgut endoderm epidermis Figure 20. Frog embryo, neural tu be stage, transve rse section through midgut. (185x) C. hog Neurula 27 (i ntermcdi.te mesodtrm) mesoderm me\.Ode rm t---;I-,L_ en doderm Figure 21. Mesoderm d ivisi ons in typical vertebrate neurula. From S. EI . Op penheimer, Introduction /0 Embryonic Development 2nd Ed (Boston: Allyn and Bacon, 1984). 28 THE FROG head ou!g rowth gilt pta!e area J,: hYfIOPhysis f.._- tr '.- Ofa l suder uu~k region , neural wOe ,', neuren!eric --, , , hd , , hd , toregut !a il bud ¥il l lo re plate timb yo lk area Figure 22. Early neura l td)e stage of the frog, Rana pipiens, 2';' to 3 mm, in length. (A) Dorsal view. (8) Midsagittal section of embryo ,imilar to (Aj. (() Same as (B). showing organ.form ing areas. Abbreviations: V. HD. '" ventral hindgut diverti (:ulum; D. HD. '" dorsa l hindgut diverticulum; PHAR. '" pharyn geal diverticulum of foregut. {OJ. Lateral view of (Aj. From O. E. Nel sen, Com parative Embryology or th e Vertebrates (New York: McGraw-Hili, 195 3). D. Frog Tailbud, 4 mm Stage notochord pharynx prosencephalon spinal cord notochord tai lbud yolky endoderm epidermis Figure 23. Frog embryo, ta ilbud stage, sagittal sectiOl1, scanning electron mi crograph. (63.9 x ) ] 0 TH E FROG tail hud epiderm is som ites otic vesicle optic cu p yolkyendoderm pha rynx adhesive st omodeum glartd Fi gure 24. Frog embryo, ta ilbud stage. sagiUJ I section (-14 .4 x) D, Frog Tailbud, 4 mm Stage 31 tai lbud epiderm is somite, midgut spinal cord mesencephalon prosencephalon pha ryn x yolkyendoderm liver diverticulum heart adhesive gland Figure 25. Frog embryo, ta ilbud stage, sagi tta l section . 05 5 xl 32 THE fROG epidermis lens yolky endoderm adhesive gland Figure 26. Frog embryo, la ilbud stage. sag ittal sect ion near outer surface . (4 4.4 x ) O. Frog Tailbud, 4 mm Slage JJ tai lbud stomodeum adhesive yolkyendoderm gland (below epidermis and mesoderm ) Figu re 27. Frog embryo. 4 mm, scanning electron micrograph . (67.2 x l 34 THE FROG prosencephalon epidermis adhesive gland pharynx yolky endoderm Fi gure 26. Frog embryo, 4 mm, sag ittal section, scan ning electron micrograph. (75 .2 x ) D. Frog Tailbud. 4 mm Stage 35 r ho mlwnc~ph "l on ~ eu , . 1 tube optic bu lge ,ectu m vent ral m~wdc r m oral evaginati on B ,ubnotochordal n ~ ur.1 lube "" notochord A c Figure 29. Structu re of 3'11 - to 4-mm, embryo of Rana pipiens (about eight pairs of somite, are present). (A) External do rsal view. {B) M idsagitta l view. (C) Same, showing major organ -forming areas. From O . E. Nel>e n, Comp,Jralivc Embryology of the Vertebra tes (New York: McGraw-Hi li. 1953). E. Frog, 5-8 mm Stages tail fin somites yolky endoderm gill adhesive gland stomodeum olfactory pit (below epidermis and mesoderm) Figure 30. Frog embryo, 5-6 mm, scanning electron micrograph. (55.9 x) developing gill gill epidermis anus Fi s u ~ 31. Frog embryo, 6_7 mm. hor izontal <.eel i<.> n, ;c,nning ell'Ctron micro graph. 159.3 x I 38 THE FROG deve loping eye brain pharynx heart gil l epidermis gill yolkyendoderm Figure 32. Frog embryo, 6- 7 mm, horizonta l section, sca nni ng electron micro graph.1144.2 x J E. Frog, S- 8 mm Stages 39 diencephalon optic cup lens vesicle gil l epidermis yolkyendoderm Figure lJ. Frog embryo, 6-7 mm, horizontal section. sca nning electron micro graph . (146.9 x ) 40 THE FROG epidermis prosencephalon Figure 34. Frog embryo, 5-7 mm, transverse section th rough prosencepha lon. (120x) Frog, 5-8 mm St;,ges 41 mesencephalon prosencephalon optic cup pharynx ad hesive gland e pidermis Figure 35. Frog embryo. 5- 7 mm, transverse section through optic cup. 1120 X) 42 THE f ROG rhombencepha lon ot ic vesicle notochord epiderm is pharynx endoderm adhesive gland Figure 3&. Frog emb r ~'O, 5-7 mm. transverse section through oti c ve sicle (120 X) E. Frog, 5-8 mm Stages 43 rhombencephalon tear artifact otic vesicle notochord epidermis endoderm pharynx artifact of slide preparation gill pericardial cavity heart Figure 37. Frog embryo, 5-7 mm, transverse sect ion through heart. (105.6x) 44 THE FROG rhombencephalon som ite notochord foregut hypomere endoderm liver epiderm is diverticulum Figure 38. Frog embryo, 5- 7 mm, transverse section through liver diverticu lum. (120 x) E. Frog, 5- 8 mrn Stage> 45 sp inal cord notochord somite midgut endoderm , epidermis Figure 39. Frog embryo, 5~7 mm, transverse section through midgut. {1 20x} 46 THE FROG • '" dorsal fin spinal cord >--_____ epidermis notochord --'-~.;....- somite ~--T--- subnotochorda l rod hindgut endoderm Figure 40. Frog embryo, 5-7 mm, transverse section through hindgut. (120x) E_ Frog, 5- 8 mm S1ages 47 tail fin gill olfactory pit stomodeum Figure 41. Frog embryo, 7- 8 mm, scanning electron micrograph. (79 x ) 48 THE FROG stomodeum olfactory pit adhesive gland __--1 gill Fisure 42. Frog embryo. 7 8 mm, SC;l rm ins electron microsraph. (1 30 x ) E. Frog, 5- 8 nlln Stagel 49 prosen cepha lon rhombencephalon somites • • . pha ryn x heart yol kyendoderm anus Figure 43. Frog embryo. 7- 8 mm, sagittal section. (32.8x ) 50 THE FROG .nte,io, , >. ante,,,,,_·; __"" lobe 0 pl'O""pllfic dvct pituit~'Y opening into the cloaca bOO, stomodaeal prt f"lt i aol1al a,ch ane,i", A. infe'io, 0' extern ~ 1 jugula, vein thi,d br~lKhial aOl1a l ar:h "~:~;;::;;"~~ A . ~ ~ len div'l,on "g,,1 uMs,on bulbus cordis Figure 44. Early frog tadpole, sketch from O . E. Nelsen, Comparalive Embryol ogy of the Vertebrates, McGraw Hill, 1953. F. Frog, t 0-t 8 mm Stages mouth heart gills '" epidermis anu. Figure 45. Frog tadpole, 11 mm, horizontal section, scanning electron micro graph. (52.3 X) 52 THE FROG pulmon~ry pulmonary do".1 inlern;iI ;lrte'Y carotid ~" rll'Ural tube , ,. coil,O/ '~udal gill 1 Or ,,"'ernal imestine artery c~rotid artery start here ventricle venosus developing inferior vena cava Aortal arc he, 3-6 function as part 0/ the also consult fig. 294, B. branchial mech~nism. Aortal . rd"" 1 and 2 are vestigial in In.. trog. ,. diagram ,howing brar>ehi.1 irllerbranChial chamber on left ,ide chamber communication arrow, r.how water currents below heM figure 46. Frog tadpole, 10-18 mm, anatomy. From O. E. Nelsen, Compara- tive Embryology of the Vertebrates (New York: McGraw-Hili, 1953). F. Frog, 10-18 mm Siages 53 head outgrowth t~i l bud gill.re~ stomodaeum A head pharyngeal outgrowth trunk '", ::e>cternal 8,:::.-ll s ~nasal- p,t ~omodaeum F oral sucker asym m ~ try of trunk H oper~ul ~ r .fOI~ ~S Ucker :+O.:tiJ!C' ~-=---=~ ~ventral fin no(ochord and muscl e mouth with horny larval tl'l'th , 1 I I I L Figure 47. External views of embryos of Rana sylva/ica and Rana pipiens. (A to J after Pollister and Moore: Anal. Rec., 68; K and L after Shumway: Anal. Rec., 78.) (A, B) Lateral and ventral views of 5·mm. stage. Muscular movemen t is evi· dent at this stage. expressed by si mple unilateral flexure; tai l is about one·fifth body length. (Pollister and Moore, stage 18.) (C. 0) l ateral and ventral views of 6·mm. stage. Primitive heart has developed and begins to beat; tail equals one· third length of body. IPoll ister and Moore, stage 19). IE, F) Similar views of 7· mm. stage. Gi ll circu lation is established; hatches; swims; tail equals one-half length of body. IPollister and Moore, stage 20.) (G, H) Ten·mm. stage, lateral and dorsal views. Gills elongate; tail fi n is we ll developed and circulation is established within; trunk is asymmetrical coincident with posterior bend in the gut tube; cornea of eyes is transparent; epidermis is becoming transparent. (Po l· lister and Moore, stage 22.) (I , J) Eleven·mm. stage, true tadpole shape. Opercu· lar fold is beginning to develop and gradually growing back over gills. (K, l) Eleven·mm. stage of R. pipiens embryo. Observe that opercu lar folds have grown back over external gills and developing limb buds; opercular chamber opens on left side of body only. From O. E. Nelsen, Comparative Embryology of the Vertebrates (New York: McGraw·Hill, 1953). II The Chick Table 2. Chick Development Hours Characterist ics Freshly laid prestreak; embryonic shield forming 6 initial primitive streak 12 primitive strea.< extend ing 18 definitive primitive streak; primitive groove and Hensen's node present 19 head process; early notochord e~tends beyond Hensen's node 20 head fold 22 neural plate begins to fold; 2 somites 24 neural folds better developed; 4 somites 27 endocardial and myocardia l tubes forming; enlarged forebrain; 7 somites 30 heart tubes fuse to form a single tube; heart ventricle begins to beat; forebrain, midbrain, and hindbrain visible; 10 somites 33 heart tube bent to right; heart ventricle and atrium beat; first pair of aortic arches prescnt; optic ves icles well defined; 13 somites 3& well developed heartbeat; auditory placode, present; pronephric tubules first a~ar ; 16 somites 40 head torsion begins; hindbrain divided; lens placodes form; lB somites 44 fiver primordium begins to appear; 22 somites 48 sinus venosus develops; 25 somites 54 two pairs of aortic arches present, third forming; hindgut present; 29 somites 60 fourth pa ir of aortic arches beginning to form; 31 somites 72 telencephalic vesicles present; dorsal pancreas evagination appears; 35 somites The student will Quickly see that there is variability in the developmenta l progress within a group of eggs incubated for a ,pecific time. This is due to many factors, including varying amounts of ilcubation before removal from the nest to begin incubation in the laboratory. This table should be useful to the student because it includes some of the major characteristics that appear at approximate times during chick development. The hours of development and the characteristics given here are approximations. Slight differences will appear i[I other similar cha rts or tables. The table was compiled b.l>ed up:m the work of: Bradley M. Patten, Early Embryology of the Chick (New York: McGraw Hill, 1971), and V. Hamburger and H. L. Hamilton, A series of normal ,tages in the development of the ch ick embryo, Journal of Morphology, 88: 49- 92, 1951. A. Chick Gastrula • ",i,n p'imi!iv~ I'oo'e formed down the midlin. primiti •••tr • • k I. ) beginning to form ") pdmiti•• groove "..,.,..y __ - --~I(..------...... pibt.'t /' ______.... ______" >"ow, ,how , ell. _:"_~=-=:":=-______'--::=-~:':::::'::::____ moving (",m the ,,~,",ction '" >uno« th,ouih the through bl ..IOIk rm hy~bl ..t primiti.e ,roo", forming middlel.ye,. '0) Figure 48. Bird gastrulation. From S. B. Oppenheimer. Introduction 10 Embry onic Development, 2nd Ed. (Boston: Allyn and Bacon, 1984). A. Ch ick Gastrula 59 notochordal process neural plate proamnion Hensen's node area pellucida primitive groove primitive folds area opaca Figure 49. Chick embryo whole mount, 18 hours. (85.1 x) 60 THE CHICK Hensen's node primitive folds area opaca primitive groove subgerminal space area pellucida (below blastoderm in area pellucida) Figure 50. Chick embryo, 16-20 hou rs, scanning electron micrograph, (161.9 x ) B. Chick, 26-33 Hour Embryos proamnion anterior neuropore head ectoderm head mesenchyme area opaca neural tube anterior intestinal portal neural fold intel'5omitic groove somite area pellucida segmental mesoderm notochord primitive knot (Hensen's node) primitive streak Figure 51. Chick embryo whole mount, 26-29 hours. {65.7xj " (.2 THE CHICK prospeclive epidermiS ,., prO.pe'live somile . nd inlermedi. te mesoderm ,. , nem.1 "'moli, ", hy""mere inte rm ed i.le spl . nchnic mesoderm mesod.r" Fi gure 52. Mesodermal separation in chick embryo. From S. B. Oppenheimer, Introduction to Emb:yonic Development, 2nd Ed. (Boston: Allyn and Bacon, 1984). B. Chick, 26-33 Hour Embryos 63 forming proper chori.,..II.n!oi, formin& omo'","j'~'~'~"~'~:::J~~~~~::~~;;~;:=:~~ mtmbr.n. c.vity: . 1I. nloi, " Ir.-embryonk "' coe lom coelom Ipl>n<'hnopleu re Figure 53. Summary diagrdm of early chick embryo wilh ils forming extraem bryonic membranes. Longitudinal view. From S. B. Oppenheimer, Int.roduction 10 Embryonic Development, 2nd Ed. (Boslon: Allyn and Bacon, 1984). .. THE CHICK foregut midgut hindgut , • • • , • , p.ncre~, : : ~ 1 234[ duodenum II I I I ..ge "- 510mich pejunum ,""""m DD D D I I) in ...!in • dOi .. ectoderm J ileum ./ I l i • Ii.", "')¥.,c re .. ___ . lIonlo;. thY <• yolk •; ", U 1Ung bud, figure 54. Endodermal derivatives. Diagram of the gut tube and it5 ou tpocket~ ings. From S. B. Oppenheimer, Inrroduction to Embryonic Development, 2nd Ed. (Boston: Allyn and Bacon, 1984). a Ch ick, 26-33 Hour Embryos 65 proamnion optic vesicle prosencephalon border of foregut mesencephalon rhombencephalon heart vitell ine vein , somite spinal cord segmental mesoderm notochord . , neural groove primitive streak • I .' vitelline plexus Figure 55. Chick embryo, whole mount, 33 hours. (40.Sx) 66 TH{ CHICK .nt.... io< neuropore ----,_ ~_---_ ~osenceph. l on opIic v... ic le ___--., ventral.oni" fOOIl cut epimyocardium cuI ectoderm trunc", aneriosu. ~~ ventricular ..... ion --1,.".- ...,,,,,;;;;, ___ ,,,,,,'1 region anlerior , ; inlestinal portal f------,,0; .plaochf>Opleure lateral m.~j."" --~f---j ---t---- r.otocnord 01 ____+ ____ neoral tube Figure 56. Diagrammatic ventral view of dissection of a 35-hour chick embryo. The splanchnopleure of the yolk.sac cephalic to Ihe anterior intestinal portal, the ectoderm of the ventral surface of the head, and the mesoderm of the pericar dial region have been removed 10 show the underlying structures. (Modified (rom Peflliss) From B. M. Patten, Early Embryology o( the Chick (New York: McGri""·Hill, 1957), B. Ch ic k, 26-33 Hour Embryos 67 rhombencephalon prosencephalon primitive streak segmental mesoderm somite • heart foregut Figure 57. Chick embryo, 33 hours, sagittal \ection. (32.4x) 68 THE CHICK somatopletlre splanchnic prospective ectoderm mesoderm prosencephalon epidermis lens somatopleure somatic splanchnopleure endoderm head foregut infundibulum optic extraembryonic mesoderm mesenchyme vesicle coelom extraembryonic splanchnopleure coelom Figure 58. Chick embryo, 33 hours, transverse section through prosen cephalon. (164.7x) B. Ch ick, 26- 33 Hour Embryos 69 head epidermis notochord prosencephalon optic vesicle prospective lens dorsal aorta ventral aorta stomodeum pharyngeal membrane pharynx Figure 59. Chick embryo, 33 hours, transverse section through optic vesicles. (185 x) 70 TH E CHICK mesencephalon dorsal aortae anterior cardinal veins foregut ventral aortae Figure 60. Chick embryo, 33 hours, transverse section through mesencephalon, scanning electron micrograph. (213 X) B. Chick, 26--33 Hour Embryos 71 rhombencephalon splanchnopleure somatic dorsal heart splanchnic mesoderm somatopleure ventricle mesoderm coelom dorsal epimyocardium endocard ium endoderm mesocardium Figure 61. Chick embryo, 33 hours, transverse section through heart. (1·59.1 x) 72 THE CH ICK rhombencephalo n extraembryonic coelom dorsal aorta notochord dorsal aorta figure 62. Chick embryo, 33 hours, transverse section through rhomben cephalon. (159.1 xl B. Chick, 2&-33 Hour Embryos 73 neural prospectille epidermis groolle fold endoderm notochord somite hypomere (epimere) figure 63. Chick embryo, 33 hours, transller:.e :.ection through somites. (179.Sx) 74 THE CHICK prospective epidermis mesoderm neural groove just beginning --I endoderm >egmental mesoderm Figure 64. Chick embryo, 33 hours, transver>e section through segmental mes oderm. (170.2 x) C. Chick, 50 Hour Embryo op( iC ectoderm metencl'phalon choroid neuromere 01 myelencephalon vt'flual aonic root 511=",,;,.- aonic ~rche, I, II, III atrium f-~C---- pharynx cardinal vein sinus """"SUS -----.\;;cc= anterior intestinal portal ------<:~C -====-:: splanchnopleure _ t somatopl!'Ure -,,,,,- lateral me!<:><"k rm roots of omphalomeMlnt",ic omphalo- -,,.."''I----j~, o~:.r-artery mesenteric anery ~=-- notochord n!'Ural twb. ---t---1;'<;!;l)!1fl~ extent of ____-\ __ -" i I portal hindgut Figure 65. Diagram of dissection of chick of about 50 hours. The splanchno pleure of the yolk-sac cephalic to the anterior intestinal portal, the ectoderm of the left side of the head, and the mesoderm in the pericardial region have been dissected away. A window has been cut in the splanchnopleure of the dorsal wa ll of the midgut to show the origin of the omphalomesenteric arteries. (Modi fied from Prentiss.) From B. M. Patten, Early Embryology of the Chick (New York: McGraw-Hili, 1957). 76 TH E CHICK primordial v~", u la r plexus of head anterior (ard in ~ 1 ""'_ aortic . ren I aortic ''''"'' __-! ____ ~ aortic'Pfout arcn fOfIII --+----.1- comm";o::': __ -.Ii~ cardinal," t-__ 1 i I posterior cafcina l vein -- t---.lj"" Figure 66. Chick embryo, so hours, vascular sys tem in anterior region, from B. M. Patten, Early Embryology of the Chkk (New York: McGraw-Hili, 1957). C. Chick, 50 Hour Enbryo 77 notochord mesence::>halon diencephalon metencephalon optic cup ganglion of cranial rerve 5 lens myelencephalon telencephalon stomodeum bulbus arteriosus (cordis) otic vesicle ---, atrium ventricle sinus venosus anterior intestina l porta l ------ ~--___' som ite Figure 67. Chick embryo, 50 hours, whole mount. D2xj 78 THE CH ICK mesencephalon rhombencephalon otic pits heart ve ntricle somites Figure 68. Ch ick embryo. about 50 hours, scan ning electron micrograph, whole embryo with horizontal section in head region . (75.5 x ) C. Chid, 50 Hour Embryo 79 } for . b,. i ~ (pr{>l.enc. ph .lon j , (midbr.inl h('ihombndb,..inn c< pha l o~1 { ::::::: : ::: : ::::~ li-- ",", cord Figure 69. Divisions of the vertebrate brain. From S. B. Oppenheimer, Intro dliClion 10 Embryonic Development, 2nd Ed . (Boston: Allyn and Bacon, 1984). 80 THE CHICK mesencephalon rhombencephalon . otic pits heart ventricle Figure 70. Chick embryo, about 50 hours, horizonta l section of he,1d. scanning electron micrograph. (154.2 X) C. Chick, SO Hour Embryo 81 myelencephalon anterior cardinal vein notochord ____-:~'" dorsal aorta pharynx ----~i¥ aortic arch mandibular process ______~:::~ maxillary process ______stomodeum optic cup diencephalon Figure 71. Chick embryo, 50 hours, transverse section through optic cup. (114.7x) 82 THE CHICK ··1, ·.i spinal cord ------;;f .. notochord ---;i~~i somite descending aorta stomach coelom ---jrt<; 'F~" common cardinal vein sinus venosus ---4ril pericardial coelom ---if-' endocardium ventricle ----~;o--~f-,; '~'-',, ______~ ' eplmyocardlum extraembryonic coelom Figure 72. Chick embryo. SO hours, transverse section through heart ventricle. (117x) C. Chick, 50 Hour Embl)'o 83 somatic mesoderm amnion notochord posterior card inal \lein amniotic ectoderm mesonephric duct somatopleure somatopleure extraembryonic coelom dorsal aorta .' midgut endoderm yolk sac mesonephric tubule embryonic coelom extraembryonic coelom Figure 73. Chick embryo, SO hours, transver>e section through mesonephric ducts. (200 x) 84 THE CHICK som ites spinal cord notochord somite epidermis ectoderm mesoderm dorsa l aortae coelom Figure 74 . Chick embryo. 50 hours, transverse secl ion Ihrough somiles, scan ning ciectrOIl micrograph. (129.6xj C. Chick, 50 Hour Embryo 85 :;emite (epimere) spinal cord epidermis somatopleure somatic mesoderm hypomere coelom mesomere notochord endoderm coelom splanchnic mesoderm splanchnopleure Figure 75. Chick embryo, 50 hours, transverse section through somites. (148.2)() D. Chick, 3-4 Day Embryos ganglion of cran ial nerves 7. 8 myelencephalon gangl ion of crania l nerve metencepha lon aud itory vesicle mesencephalon gangl ion of crania l nerve 9 diencephalon ganglion of cranial ------f optic cup fle lve 10 lens ves icle somite , telencepha lon atrium ----- bu lbus cordis vent ricle spinal cord wing bud vitelline vessels leg bud Figure 76. Ch ick embryo, whole mount. 3 day,. {1 9.8 X ) D. Chick, 3-4 Day Embryos 87 spinal cord amniotic cavity extraembryonic I coelom somite chori on otic vesicle acoustico-facial is ganglion myelencephalon neuromere amnion , I metencephalon head mesenchyme mesencephalon Figure 77. Chick embryo, 3 days, transverse section through otic vesicles. (64.2x) 88 THE (HICK eye cup lens mesencephalon anterior cardinal veins interna l carotid arteries stomodeum mandibular process foregut amn iotic cavity descending notochord spinal cord chorion amnion aorta figure 78. Chick embryo, 3 day" transverse sectioll through developing eye, scanning electron micrograph, (61.2 x ) o Ch ick, 3- 4 Oil)' Embryos 89 coelom ductus venosus sp inal cord notochord amn ion chorion descending aorta posterior cardinal veins duodenum liller vent ricle Figure 79. Chick embryo. J days, transverse section th rough heart ventricie, sca nning electron micrograph . (97 x ) 90 THE CHICK amniotic cavity amn ion notochord spina l cord chorion descending aorta posterior ca rdinal veins duodenum P'--"';":-J~ liver L~,",,' ventricle ductus venosus Figure 80. Chick embryo, 3 days, tran>verse s.ection through ductus venosus, scanning electron micrograph. (145.7 x ) D Chick. 3-4 D genital ridge >pinal cord mesonephric duct and descending tubules aorta posterior mesentery card inal vein midgut coelom wing bud apical ectodermal ridge Figure 8 1. Chick embryo. 3 d,lYS. transverSe section through wing bud>. 5C paired dorsal hindlimb apical notochord spinal cord aortae mesonephric duct bod ectodermal ridge -, , .,"': f . f .t" ., ".r t ' _. ,.;J • .,' .i ' ..:if ' hindlimb apical hindgut embryonic coelom allantois extraembryonic yolk sac bod ectodermal ridge coelom Figure 82. Chick embryo, 3 days, transverse section through hindlimb (leg) buds. (101 x) D Chick, 3- 4 Day Embryos 93 diencephalon al lantois heart coelom posterior cardinal veins descending aorta spinal cord Figure 83. Chick embryo, 3- 4 days, transverse section through brain and spinal cord, scanning electron micrograph. (46.5 x) 94 THE CHICK sp inal cord notochord posterior cardinal vein amnion dorsal "," !,...,~ mesonephric subintestinal allantois figure 84. Chick embryo, 3- 4 days, transverse section through hindgul and al lantois, scanning electron micrograph . (8 1.4 x) D. Chick, 3-4 Day Embryo. 95 otic ves icle chorion and amnion myelencephalon I optic cup lens vesicle somites alla ntois leg bud branchial arches heart wing bud mandibular arch Figure 85 . Ch ick embryo. 3- 4 days, sagi ttJI section, scanning cicoron micro graph. (35 .2 x ) 9f> THE CH ICK metencephalon mesencephalon mye len cepha lon allantois mouth mandible pharynx descending aorta notochord heart spi na l cord hindgut telen cephalon wingbud Figure 86. Ch ick embryo. 3- 4 da ys, sagiua l section and transverse sect ion through hindgut, scan ning clcctron micrograph. (3 1.7 x ) D. Ch i c~. 3-4 Day Embryos 97 diencephalon pharynx telencephalon conus arteriosus allantois atrium ventricle sinus venosus somites leg bud wing bud Figure 87. Chick embryo, 3-4 days, sagittal section, scanning electron micro gral"lh. (27.6x) 98 THE CHICK heart atrium heart ventricle sinus venosus figure 88. Chick embryo, 3- 4 days, sagi tta l section of heart chambers, scan· ning electron micrograph. (1 41 xl 100 THE CHICK e ' !<~mal carotid artery aortic af(h III Msilar artery ''',,,,,',,,"''i artery vertebral,",," ' ~~~==j=;I-; cervical segmental anterior caminal Common caminal ,. _, posterior card i",,1 5ulxlavian vein sulxl.vian ane ry omphalomesenteric ,ubu,dinal " "" ._ v~elline vein " subintestinal Figure 90. Ch ick embryo, 4 days, circulatory system. From B. M. Patten, EM/y Embryology of the Chick, McGraw-Hili, 1957. D_ Ch ick. 3- 4 Day Embryos 101 branchial clefts at ri um conus arteriosus leg bud heart ven tricle wing bud som ites Figure 91. Chick embryo, 3- 4 days. whole. scanning electron microgra ph. (33.1 x) 102 THE CHICK Figure 92. Ch ick embryo. 3- 4 da y~ . ,agillal section. scann ing electron mino_ graph. (J2.2 x ) D. Chick, 3-4 Day Embryo> 103 heart, anterior vitelline vein ~",_~ t\\,\ vitelline arteries and vitelline veins posterior vitelline vein vitelline arteries and vitelline veins Figure 93. Ch ick embryo, 4 days, whole mount showing vitelline circulation. (73 x) III The Mam I A. Cat and Rat Gonads connective tissue young Graafian follicle dormant primary follicles tunica albuginea Graafian follicle Figure 94. Cat ovary. (71 x ) 108 THE MAMMAL follicular cavity theca interna oocyte cumulus oophorus stratum granulosa Figure 95. Graafian follicle of cat ovary. (268.7x) A. Cat and Rat Gonads 109 re~idual bodies spermatlds lumen - seminiferous tubule primary spermatocy:es mature sperm spermatogonia Figure 96. Seminiferous tubule of rat testis. (368 x) B. Pig. 6 mm Embryo tongue metencephalon hyo id arch i mouth '------' 1 telencephalon '--::"'--- atrium mandible -----:,...,~;;.~ descending aorta ventricle • , • figure 97. Pig embryo, 6 mm, sagittal section. (26.6 x) B. PiS, 6 mm Embryo 111 metencephalon tongue myelencephalon 11·_'''''=<·~ r '~~~ I-~ mesencephalon diencephalon mandible 'f pericardial cavity telencephalon , , atrium , lung bud t " . A ventricle , ,'< stomach .\, live r descending aorta ,"" "\ '--- spinal cord " , mesonephros Figure 98. Pig embryo, 6 mm, sagittal section. (23 x) 112 THE MAMMAL metencephalon tongue • mesencephalon ----j diencephalon -----' mandible mouth telencephalon ------7 atrium pericardial cavity ----'.-"----SO-----{ ventricle liver somites hindlimb bud spinal ganglia mesonephros spinal cord descending aorta Figure 99. Pig embryo, 6 mm, sagittal section. (22.7 x) c. Pig, 10 mm Embryo auditory ve,icle superior ganglion of ninth i 8Jnglion of ~ ; ght h n ~ rve aortal arch jugular gangl ion of tenth ganglion of ,eventh nerve semilunar ga ngl ion basila r filth nerve ~cc~""Y ganglioo fourth cra ni .1 ~ orta l arch III nerve aort~ 1 ""," '", dorsal root ganglion of first cervical nerve internal aortal arch carotid artery r-' """ arch t ~ocOO ,ubc l ~v ; a n _,~"" coeliac"'" dor .. 1 =_ ::~.~::':' ., 1~ lI antoicl pancre~, gall bladder ventr~1 _-\~(J' p ~nc rt ~s ,m.'''' ~ intestine diverticulum intersegmental artery ',",~,"""",, duct ~ rte ry (fulure ,uperior glomerulus meso neph ric tubule me""n!eric artery) figure 1 00. Pig embryo, 10 mm, reconstruction. From O. E. Nelsen, Compara ti \'e Embryology of the Vertebrates (New York: McGraw-Hili , 1953). 114 THE MAMMAL foramen thin roof notochord ~ricard j a l """.pocket chiasma right ~trillm tell'ncepha lon v~lve s of lamina terminali, sinus venosu. ~::S:,~:'::~ ,in", pt'rkardial coelom spinal cord "1'-___<.~":;.;m::~~1 body wall posterior vena ). transversum ductus dorsal , paocreas f.. ~;;:;:'·1,;;:, I, coelom cord :-••" .."" diverticulum ; , dorsal proctodaeum pelvis metanephric k;dney Figure 101. Pig embryo, median section of 10 mm embryo. From O. E. Nei sen, Comparative Embryology of the Vertebrates (New York: McGraw-Hili, 1953). C. Pig, 10 mm Embryo 115 capitis intermlexternal carot icarQ{idd artery~ ~~~C'-\-:-\--"'::::::::"'~ aortic arch aortic arch 6 ""rtebral cervi",,1 segmental artery common , .. rdinal ""in -t+---~~L Sllbcla~i a n artery subcla~ian coeliac omphalomesenteric (~ i telline) ".'''~ omplwlomesenteric (~ i tel(i"") ".N"" poS(erior cardinal umbilical artery fisure 102. Reconstruction of the circulatory system of a 9.4 mm pig embryo. From B. M. Patten, Embryology of the Pig, third edition (New York: McGraw Hill, 1959). 116 THE MAMMAL 1, ~, _ .-._ _ I -l - - ~ .. -- -. "'~ ---, ~ ,1 i '-'''-~ lens __~ . eye cup ___~ - , pericardial cavity ./ r - "\ ./ '-'-, ______'"-...... -- ventricle '. mesonephric glomeruli ..:;...__ mesonephric tubules _-',__ ..;.~..., hindlimb bud spinal cord descending aorta spinal cord figure 103. Pig embryo, 10 mm, sagittal section. (22.2x) C. Pig, 10 mm Embryo 117 aorta mandi ble amnion ______-,- ':':--"'l metencephalon pharynx ____ mesencephalon sp inal cord ___ '-+-4 mouth at ri um '--7''-----i bulbus cordis ri"""""=---~"':l telencephalon ~":'i:"":::':L'-----~., ventricle liver :-___~ intestine spinal ganglia '=::::::'~ mesonephric tubules --.; '1"0;,1 cord mesonephric glomeruli hind li mb bud Figure 104. Pig embryo, 10 mm, sag ittal section . (21.5 x) pl,.,.,.n< tonSO" :;~;:;:;= dm~r>Coph.Jon,ndibi< . >"n , 1c ",d ___-'\ " ,pn,1 cord fj~"rc lOS. Pi~ cmI"yo. 10 m", . .. ~itt.11 ='i",. 'lO.9 x l C. Pig. 10 mm Embryo 11 9 aortic arch 3 metencephalon branchial cleft 3 e~--.'7---- pharynx ,---: :""":l:':::'---'-- hyoid arch ""~ ______tongue I descending aorta ____ '-....",c...---- mandible atrium ___--, -,~ ____ telencephalon 1------ventricle mesonephric glomeruli y mesonephric ___-'; tubules ~-" hindl imb bud spinal cord spinal cord descending aorta Figure 106. Pig embryo, 10 mm , sagittal section. (22.2x ) 120 THE MAMMAL pharynx metencephalon __- hyoid arch aortic arch descending oort,---- mesonephric tubules so mites --~'" mesonephric _____ glomeruli ""-"';,,pln, '1 cord \ hindlimb bud Figure 107. Pig embryo, 10 mm, sagittal section. (20.6 x) C. Pig. 10 mm Embryo 121 myelenceph~lon metencephalon head mesenchyme mesencephalon Figure 108. Pig embryo, 10 mm. transverse section through midbrain and hindbrain. (65 x) ~------"' .. ~"'."",.,. !f------ J -""" ..,., ...... ,... ~ ,.".., • . IU ",", , ...",,., ..... ,,"" ",... "" _ , ••...1 •. '" .) C. Pig. 10 mm Embryo 123 :-______myelencephalon . - ____--' crania l nerve 11 _____ crania l nerve 12 ____ cranial nerve 12 ____ cranial nerve 11 ____ cranial nerve 10 cranial nerve 9 cranial nerve 9 otic vesicle anterior cardinal vein acoustic ganglion 8 crania l nerve 7 geniculate branchial groove ganglion 7 pharyngeal pouch 1 basilar artery semilunar dense mesenchyme ganglion S anterior ca rdinal vein semilunar ganglion S ____ internal carotid artery diencephalon Figure 110. Pig embryo, 10 mm, transverse section through diencephalon and myelencephalon. (37.7 x) 124 THE MAMMAL ependymal layer • of spinal cord --""", cord '.m"II, layer of spinal cord , I ganglion ,. / pharynx left dorsal aorta left anterio r cardinal vein mandibular f-,---':"'-- ventral aorta maxillary P"''''''-- =------branchial groove II ''",,'" ( layer • Figure 111. Pig embryo, 10 mm, transverse section through a developing eye. (32.8x) C. Pig, 10 mm Embryo 125 ependymal layer of spina l cord spina l cord spinal gangl ion manlle (ayer of spina l cord anterior cardina l vein dorsal aorta pharynx pharyngeal pp 'cd, _~ branchial groove mandibular ramus of cranial nerve 5 mar"ldibular process mouth optic ~~.~ .. '~ __ lens ",;,1, ''-, __ maxillary process diencephalon layer optic cup Figure 112. Pig embryo. 10 mm, transverse section through maxillary i\ lld mandibular processes. (37.7 X) 126 THE MAMMAL ;"--::--'--'---l ependymal layer of spinal cord --~--'l spinal ganglion ~-----'l mantle layer of spinal cord --,..,,:---i myotome ---"---'l sclerotome right dorsal aorta f---- ,--_--, left dorsal aorta ----' pharynx cardinal , left anterior cardinal vein right atrium ::--j,"'--~T epidermis of body wall &[2~~~'I.~c..:_f.:J, conus arteriosus "CF----/f- left atrium fhiL----.--, pericardial cavity olfactory pit Figure 113. Pig embryo, 10 mm, transverse section through heart chambers. (38.5 x) C. Pig, 10 mm Embryo 127 right common cardinal vein dorsal aorta right subclavian vein ependymal layer of spinal cord spinal cord '"'..,_ dorsal root of spinal spinal ganglion mantle layer of spinal cord dorsal aorta cardinal vein trachea right ",'orr.---~ , -. "--.I left atrium bu lbus cordis olfactory pit -, ...- .~ . Figure 114. Pig embryo, 10 mm, transverse section through olfactory pit and heart chambers. (33.2 x) 128 THE MAMMAL right dorsal aorta spinal cord right common cardinal 'r'odym,' foreleg bud mantle layer of ---spinal cord .,",<""b,d dorsal aorta right horn of cardinal vein sinus ,"eo,"" -----__.,.~ valve of sinus venosus "','d'o!'---~-,"'---__-t~ .. ____ left horn of sinus " venosus ------left atrium right endocardial right atrioventricular ----'l canal interventricular right ventricle -----\ ~~~~~~~rf-r------left ventricle ~ 7------p"'",·,,,' cavity .. . ' 01f.",,"1 pit interventricular sulcus Figure 115. Pig embryo, 10 mm, transverse section through foreleg buds and heart ventricles. (33.2 xl C. Pig. 10 mm Embryo 129 sp inal ganglion mantle layer foreleg bud righ t dorsa l aorta right left dorsal aorta card inal vein pleural cavity bronchus left posterior card inal vein epiderm is sinus venosus • left ventricle right ventricle • pericardial cavity ventricular septum Figure 116. Pig embryo. 10 mm, transverse section through heart ventricles and bronchi. (37.7 x ) 130 C. Pig, 10 mm Embryo spinal epidermis ------0:'1"'~------~:::::'1 root spinal nerve mantle ______==;;;::- laye r brachial plexus foreleg bud descending aorta mesonephros esophagus left stem bronchus apical ectodermal ridge ----''-liver septum traosversum ventricle figure 117. Pig embryo, 10 mm, transverse section through liver. (3 4x ) TH E MAMMAL 131 spinal cord subcardinal anastomosis peritoneal cavity epid ermis glomeruli , '. \ ~ \ T1 esonephri c duct descending aorta notochord apical ectodermal ri dge common iliac arteries Figure 11 S, Pig embryo, 10 mm, transverse section through mesonephros. (35.2 x) D. Human Development Table 3. Some Major Characteristics of Human Development Wet!k Characteristics 1 Fertilization, cleavage, morula, blastocyst, implantation begins, endoderm of embryo visible 2 Embryonic disc is bi laminar, amniotic cavity appears. implantation complete, primitive placental circulation established 3 Primitive streak forms, gastrulation occurs, neurulation begins 4 Heart begins to beat, neural folds fusing. eye and ear primordia presen t, 4 pairs of branchial arches, arm and leg buds prescnt 5 Lens vesicles, optic cups, nasal pits form; hand and foot plates are paddle shaped; heart atrium dividing 6 Oral and nasal cavities confluent, upper li p formed, arms bent at elbow, fingers distinct but webbed, palate developing 7 Eyelids forming, tip of nose distinct, genital tubercle, urogenital and anal membranes form, trunk elongating and straightening 8 Upper limbs bent at elbows, fingers distinct, anal membrane perforated; urogenital membrane degenerating, testes and ovaries distinguishable, externa l genit~li~ indifferent but beginning to diffe renti~te, ~U e5Sential external and internal structures h~ve begun to form 9 Begins fetal period, genitalia differentiation begins 10 Face has human appearance, genitali~ begin to ,how dist inct male or female ch~racteristics 11 Growth ~nd e l ~bor~tion of all structures continues; at about 12 weeks the sex of the fetus is externally distinguishable 5 weeks 1 week 6 week' 7 weeks 3 w~ ks 6 weeks 36 weeks figure 119. Summary of human development. 133 134 THE MAMMAL thalamus mesencephalon cerebellum cerebral hemisphere pontine flexure myelencephalon diencephalon epidermis epiglottis pharynx C'1c---'-, esophagus tongue mouth sternum heart forelimbs (hands) '" I", liver , spinal cord centrum of vertebra hindlimbs (feet) Figure 120. Human embryo, 25 mm, about 8 weeks, sagittal section. (73 x ) pp I Planes and Sections Terminology Used in this Atlas "'gitta l plane, frontal norizontal tranlVe ~ Or cross plane, yielding ",gitl~1 SKlion plane. yielding fronta l yielding tranwe~ Or Or horizontal ~ ti on crms section Obtaining Frog Embryos for Microscopy for this Atlas Ma le and female leopard frogs (Rand pipiens) were obtained from commercial dealers. Frogs were ,tored at 4°( unt il rcady for use, at which time they were transferred to room temperature. Female frogs in prebreeding condition were inoculated with frog pituitary gland extract obtained from Carolina Biological Supply Company to induce ovL'lation. This pxtract, made from dried pituitary glands, was mixed with distilled water and then injected into the abdomina l cavities of the fem",le frogs . Eggs were released (.Ifripped) from the female frogs and fertilized by gently squeezing the frogs over a sperm suspension prepared by mincing frog tes tes in spring water or 10% Holtfreter's solution or 10% Amphibian Ringer's solution (formu lae given in this appendix) . The fertilized frog eggs were mJintained in spring water or one of the above mentioned 10% >olutions at room temperaturc. Development proceeded acturding to the timetable givcn earlier in the text. At selected times, embryos were placed in buffer and fixative and prepared for microscopy. Obtaining Chick Embryos for Microscopy for this Atlas Chick eggs at varioos stages of development were cracked into ringer bowls containing Howard Ringer's solution (formula in this appendix). The blastoderm, or ch ick embryo proper, is seen as a whitish colored disc that lies atop the yolk. The blastoderm was removed from the yolk by cutting around the entire blastoderm with a pair of scissors and gently peeling it off the yolk into the Ringer's solution. The vitelline membrane was usually removed from the blastoderm if it was still attached after the blastoderm was removed from the yolk by gently teasing it loose around the edges of the blastoderm and lift ing it away. The blastoderm was then placed into buffer and fixative by sucking it out of the Ringer' s solution with a wide-mouth pipette. Preparation of Specimens for Scanning Electron Microscopy for this Atlas Th e embryos used for the scanning ele.:;tron microgra phs were placed in O. IM sodium cacodylate buffer so lution (pH 7.2-7.3) and fi xed in 2.5% glutaral dehyde, 4% paraformaldehyde and 0.0750/.. (aCi, in U.1M sodium cacodylate buffer for 8-24 hours al 4°(, They were the n washed overnight al 40C in U.1M sodium cJcodyl Armstrong, p, B , A sc~nning electron microscope techn ique for study of the internal microanatomy of embryos, Microscope 19:281 - 284 (1971 L Armstrong, P.B. and D. Parenti, Scarming electron microscopy of the chick embryo, Dcvclopl7"lental Biology 33:457--462 (1973). Karnovsk'{, M.J., A formaldehyde-glutaraldehyde fixative of high osmolal ity for use in electron microscopy, Journal of Cell Bioi08)' 27:137A- 138A 11965). Light Microscopy Equipment Used for this Atlas Sections larger than 4mm in diameter were studied and photographed with a Wild M-S stereomicroscope and a Nikon F2A camera. All other ~tions were studied and photographed using a Zeiss Photomicroscrope I. Panalomic-X (ASA 32) 35 mm film was used for all micrographs. We thank Professors Anthony Gaudin, Daisy Kuhn, and George Lefevre for permitting us to use their equipment. , Holtfreter's Solution An amphibian Ringer's solution that is usually used at 10% strength for culturing amphibian material. Full Strength Formula Component Quantity Nae! 3.5 gm KCI 0.05 gm Caell 0.1 gm NaHCOJ 0.2 gm Distill ed water 1000 ml Amphibian Ringer's Solution I\n amphibiJn Ri ngcr"s sol ution that I, lbUdll )' uled At 10",(, st rength io r cuitu rl nr; 'lmphi hian materia l. Ful l Stre ngth f orm li ia Component Qu,lnlit y NaC I 6.60 gm KCI O. l 'igm C 1CI, 0.15 gm NaHCO , enou);h to adjust pH to 7.8 Distilleri w ater 1000 ml Howard Ringer's Solution This is a good isotonic sa line solution for use with living chick material. Component Quantity NaCi 7.2 gm CaCl 2 (2H ~ O) 0.178m (or 0.23 gm) KCI 0.37 gm Distilled water 1000 ml - • Glossary acoustic g,mglion 8: Ganglion of cranial nerve 8. adh~ive gland: Ectoderma l thicken ing on the ventral side of the head of frog tadpoles used for attachment to a substratum (such as rocks, plants, etc ) allantois: Extraembryonic sad ike e~ten s ion of the hindgut of amn iotes, serving excretion and respiration. amnion: Extraembryonic membrane of amniotes, inside the chorion, composed of somatopleure. amniotes: Vertebrates possess ing an amnion during development. amniotic cavity: Space between amn ion and embryo proper. anim;!1 region (or 3nimill hemisphere): Region of egg where the nucleus resides, opposite the vegetal region. anterior cardin.. 1 veins: Primitive paired veins of the head . anterior intestinal portill: Opening from midgu t into foregut in amniote5. anterior neuropore: Temporary opening into neu ral tube. anus: Posterior opening of the digestive tube. aorta: Main trunk of the arterial system. aortic arches: Paired arteria l connections between the dorsa l and ventral aortae. apical ectodermal ridge: Ectodermal thickening on limb bud tip. area opaca: Peripheral zone of the chick blastoderm which is attached to the yolk below. area pelludda: Relatively transparent central region of the chick blastoderm underlaid by the subgcrminal space. archenteron: Primitive embryonic digestive tube. archenteron roof: The dorsal covering of the archenteron that becomes the notochord. ascending aorta: Portion of aorta that extends anteriorly from the heart. atrioventricular canal: Passage connecting the heart atrium and ventricle. atrium (of heart): Heart chamber that delivers blood to the ventricle. In the mammalian heart, the ri ght at ri um receives venous blood from the body and delivers it to the right ventricle. The left atr ium receives oxygenated blood from the lu ngs via the pulmonary vein and delivers it to the left ventricle. i 146 GLOSSARY branchial arches: Series of paired bars in the wall of the pharynx, that give rise to structures including parts of the jaws, skull, and middle ear. branchial clefts: Series of paired perforations in the wall of the pharynx that separate the branchial arches from each other. branchYi srooves: Paired ectodermal invaginations in the wall of tile pharynx. Each groove corresponds to a branchial (pharyngeal) pooch. branchial pouches: See pharyngeal pouches. These are endodermal evaginations of the lateral wall of the pharynx thai form parts of the middle ear, tonsil, thymus, and parathyroid glands. bronchus: Respiratory tube connecting the tracilea with the lungs. bulbus arteriosus: See conus arteriosus. bulbus cordil: See conus arteriosus. chorion: Outermost extraembryonic membrane of amniotes, composed of s0- matopleure; also used to describe a surface coat exterior to the plasma membrane in the eggs of fishes and tunicates. coetom: Body cavity. common cardirlOll vein: Trunk of the anterior and posterior cardinal veins connecting the sinus venosus. common Iliac ~rterin: Large terminal branches of the aorta. conus arteriosus: (bulbus arteriosus, bulbus cordis) Anterior most portion of the heart, connecting the ventricle with the ventral aorta. comea: Transparent front covering of the eye. cranial nerves (c.n.): nerve pairs arising from the brain. c.n. 3 innervate all inner eye muscles and some extrinsic eye muscles (also called oculomotor nerve). c.n. 4 innervate superior oblique ocular muscles (also called trochlear nerve). C.n. 5 innervate mandibular arch region (also called trigeminal nerve). c.n. 6 innervate external rectus eye muscles. c.n. 7 innervate the hyoid arch. c.n. 8 innervate the Inner ear (also called the vestioo/ocochlea.r nerve). c.li. 9 innervate the third branchial arch (also called glossopharyngeal nerve). c.n. 10 innervate branchial arches 4, S, 6. In the frog tadpole inne1'Vate the lateral line (which forms sense organs in the epidermis) (also called vagus nerve). c.n. 11 innervate muscles of shoulder and pharynx (also called accessory nerve). c.n. 12 innervate tongue muscles (also called hypoglossal nerve). wmu.... oophorus: Follicle cell layers of stratum granulosa surrounding the oocytes of mammals. dense iLkKhch)m,,: groups of mesenchyme cells (embryonic connective tissue) that will form cartilage. dennatome: Quter region of the somite that gives rise to the dorsal dermis of the skin. descendlnl aorta: Main trunk artery formed by fusion of the paired dorsal aortae. diencephalon: Posterior portion of the forebrain, that forms the thirst center (thal amus), hunger center (hypothalamus), the posterior pituitary gland, and the optic vesicles. donnant primary follicles: Small capsules inside tile outer ovary wall of mammals, each containing an immature oocyte and follicle cells. GLOSSARY 147 dorsal aortae: Paired arteries which fuse together posterior to the pharynx to fo rm the descending aorta. . dorsal lip of the blastopore: prospective notochord; th e fir)t reg ion to enter the amphibian embryo during gastrulation. dorsal mesocardium: Dorsal mesentery (supporting membrane) of the heart. dorsal root of spinal nerve: Dorsal portion of sp inal nerve connecting the nerve trunk with the alar plate (dorsa l la teral wall) of the sp inal cord . e<:toderm: Outer germ layer (original part) of the embryo. endocardial cushion: Connective tissue ring that fo rms the valves in the canal between the heart at ri um and ventric le. endocardium: Inner lining of the heart. endoderm: Innermost germ layer of the embryo. endolymphatic duct: Sta lk of the otic vesic le. ependymal layer: Inner layer of primitive neuroepithe li al cells (inner surface nerve ce ll s) of the neural tube. epidermis: Outer epithelial (surface) portion of the skin. epimere: somite; dorsal reg ion of mesoderm consisting of myotome, dermatome, and sclerotome. epimyocardium: Outer la yer of heart. esophagus: Digestive tube connecting pharynJl with stomach. extraembryonic coelom: Cavity outside the embryo proper th at is continuous with the body cavity (coelom) and is surrounded by extrae mbryonic membranes. fertilization membrane: a coat that forms at the su rface of eggs during fertil ization. follicle cells: Cells surrounding oocytes that help nourish and protect the developing oocytes. follicular cavity (antrum): Space inside of the Graafian follicle filled with tlu id. forebrain: Anterior most portion of the bra tn. foregut: Anterior portion of the gut tube. which connects with the midgut and forms the pharynx (and its derivatives), stomach. and duodenum. ganglion: A group of nerve cells whose ce ll bodies are located outside the centra l nervous system. geniculate ganglion 7: GangHon of the seventh cran ial nerve. genital ridge: Thickening of posterior mesoderm that will fo rm the gonad. germinal vesicle: Enlarged nucleus of the oocyte. Graafian follicle: Capsu le in th e mammaHan ovary. conta ining a folHcular cavity. an oocyte, and follicle cells. 148 GLOSSA RY inferior vena cava: Ma in trunk vein , infundibulum: A ventral evagination of the prosencephalon. internal carotid arteries: Exten.ion. of the dorsa l aortae that provide th e ma in arterial blood supply to the brain. intersomitic grooves: Spaces separati ng somites. interventricular foramen: Opening beM'een the right and left ventricl es of th e heart. interventricular sulcus: Groove on the surface of the heart ventricle ma rk ing the plane of its impending div ision into left and right ven tricles, intestine: Portion of the gut tube posterior to the stomach. larynx: Voice box leg bud: Rudiment of leg lens: light-focu si ng structure of the eye. lens placode: Thickening of head epidermis that will form the lens of the eye. lens vesicle: Sac resulting from an invagi nation of the lens placode whi ch will form the eye lens. limb bud: Rudiment of limb. liver diverticulum: Evagination of gut tha t gives rise to the live r, gall bladder, and common bile duct. lumen: Inner passage of a tu bular structure. macromeres: large cleavage blastomeres. mandible: lower ja w. mandibuliH arch: Branchial arch I. mandibular process: Posterio r division of mandibu lar arch , mandibular ramus of cranial nerve 5: Poste rior portion of cranial nerve 5, innervat ing the mandible and jaw muscles. mantle layer: Midd le layer of developing neu ral tube. maxillary process: An terior portion of the mandibular arch. meiosis: Divisions of the germ cell line that eventually resul t in the fo rmation of haploid gametes. mesencephalon: Midbrain. mesenchyme: EmbryoniC connective tissue. mesoderm: Middle germ layer (orig inal part) of the embryo. mesomere: Intermediate mesoderm between epimere and hypomere: also used to de.Gibe medium-sized cleavage blastomeres. mesonephric duct: Duct connecting mesonephric tubules and cloaca. mesonephric glomeruli: Capilla ries within Bowman's capsules (invaginated kidney tu bules) of the mesonephros. mesonephric tubules: Kidney tubu les of adult fish and amphibians, and of embryonic birds and mammals. metencephalon: Anterior port ion of hind brain, whi ch gives ri.e to the cerebellum of the brain. micromeres: Small cleavage blastomeres. midgut: Area of digestive tube or prospe<: tive digestive tube between fo regut and hindgut. which forms the jeju num and ileum (po rtions of the small intestine) and the anterior porti on of the la rge in testine , GLOSSA RY 149 mouth: Anteri or opening of the digestive tube. myelencephalon: Posterior portion of hindbrain, which form~ the medulla of the brain. myotome: Somite division that forms the ~ke l etal muscle of the body wall. neural folds: Elevated ridges of the neural plate. neural groove: Trough formed by the bending up of the neural plate. neural plate: Embryonic region that becomes the nervous system. neural retina: Sensory retina . neural tube: Tube derived from the neural plate that forms the nervous system. neuromeres: Constricted minor segme nts of the brain. notochord: Fibrocellular rod con~tituting the primitive skeletal axis. nuclear membrane: Membrane surrounding the nucleus. nu cleolus: Dense granule containing ribosomal RNA and proteins, found in the nucleus of cells. Site of ribosome assembly . nucleU$ ; Cell ular organelle containing the chromosomes and usually one or more nucleoli. olfactory pits: Cavities on the lateral reg ion of head, arisi ng by invaginati on of the olfactory placodes, that will form the nasal cavities. olfactory placod€5: Ectoderma l thickenings on the latera l regions of the head that eventually form the nasal passages. oocyte: An immatu re egg, developi ng from the oogonium. that through growth and meiosis gives rise to a mature egg. oogonia: Primordial egg cells that give rise to oocytes and eggs. optic cup: Invaginated outpocketing of the diencephalon of the brain that forms the neural retina and pigmented coat of the eye. optic stalk: Connection of the optic cup to the diencepha lon. otic placode (ear placode; auditory placode): Thickening of head epidermis that eventually forms the inner ear. otic vesicle (ear vesicle; auditory vesicle): Chamber formed from invagination of the otic placode which will form the inner ear. pericardial coelom (pericardial cavity): Cavity around the heart. pha ryngeal pouches: Paired evaginations of the lateral wa ll of the pharynx. pharynx: Anterior portion of the foregut . pigmented layer (of eye): Outer wa ll of optic cup, forming a light-tight coal. pleural cavity: Body cavity surrounding each lung. posterior cardinal veins: Primi tive paired veins of the trun k situated dorsal to the mesone phros (the functiona l kidney of adult fish and amphibians). primary oocytes: Cells arising as a result of growth and DNA duplication in oogonia. primary spermatocytes: Cells aris ing as a result of growth and DNA duplication in spermatogonia. primitive knot: See Hensen·s node. primitive streak: Thickening in the surface of some embryos at the beginning of gastru lation. 150 GLOSSARY proamnion: Cresent-shaped area around the head of early bird embryos. prosencephalon: Forebrain. prospective (presumptive) region: The region of an early embryo that will become a specific structure in the embryo's later development. residual bodies: Particles of cytoplasm discarded by the spermatids as they dif ferentiate into mature sperm. rhombencephalon: Hindbrain. sclerotome: Medial somite region that gives rise to the vertebral column. secondary oocyte: A meiotic product of primary oocyte. secondary spermiltocyte: Product of the meiotic division of a primary'spermatOCyte. segmental mesoderm: Prospective somites. semilunar ganglion 5: Ganglion (aggregation of nerve cells) of cranial nerve 5. seminiferous tubules: Sperm-forming tubules of the testis. 5ertoli cells: Cells in the testis that support and nourish developing sperm. shrinkage artifact: Separation of cellular components or tissues due to the preparation of the material for study; absent in the living organism. sinus venosus: Posterior chamber of the embryonic heart that receives venous blood. somatic mesoderm: Hypomere mesoderm in close contact with ectoderm. somatopleure: Combination of somatic mesoderm and ectoderm. somite: Epimere; dorsal region of mesoderm consisting of myotome, dermatome, and sclerotome. Epimere or somite consists of segments of mesoderm termed somites. sperm (spermatozoan): Mature male gamete. spermatid: Product of the meiotic division of a secondary spermatocyte. spermatocyte: Stage in the maturation of the male gamete preceding the spermatid stage. spemIiltogonium: Primordial sperm cell that gives rise to spermatocytes and sperm. spinal cord: The portion of the central nervous system posterior to the brain. spinal ganglia: Ganglia on the dorsal roots of spinal nerves. splolnchnic mesoderm: Hypomere mesoderm in close contact with endoderm. splanchnopleure: The combination of splanchnic mesoderm and endoderm. stomach: Enlarged section of the foregut posterior to the esophagus. stomodeum: Ectodermal invagination that forms the mouth cavity. stratum granulosa: Follicle cell-derived layer surrounding the inside of large ovarian follicles. subcardinal anastomosis: Medial interconnection between left and right suocardinal veins. subgenninal space: The space between the chick embryo blastoderm and the underlying yolk. GLOSSARY 151 tail bud: Rudiment of the tail and posterior trunk of an embryo. tail fin: Blade-like extension of the tail edge in amphibians. telencephalon : Anterior portion of the forebrain. theca edema: The outer layer of the amphibian oval)'; the outer layer of mammalian Graafian follicles. th eca interna: A layer containing blood vessels, connective tissue, and endocrine glands, situated between the theca externa and the stratum granulosa of large ovarian follicles. trachea: Tubular connection of Iilf)'nx (or lal)'ngotracheal groove) and lung bronchi. tunica albuginea: Fibrous connective tissue covering the oval)' and testis. vegetal region (vegetal hemisphere): Region of egg, opposite the animal region; yolk often accumulates in the vegetal region. ventral aorta: Outlet of the embryonic heart that lies in the floor of the pharynx and conducts blood from the bulbus cordis (bulbus arteriosus, conus arteriosus) to the aortic arches. ventral lip of blastopore: Lower or belly region adjOining the blastopore; last region to enter the blastopore during amphibian gastrulation . ventricle (of heart): Thick waned heart chamber that receives blood from the atrium. In the mammalian heart, the right ventricle delivers venouS blood from the right atrium to the lungs via the pulmonary artery. The left ventricle delivers oxygenated blood (from the lungs and left atrium) to the body via the aorta. ventricular septum: Muscular partition between the right and left ventricles. wing bud: Wing rudiment. yolk plug: The center of the circular blastopore in amphibian embryos, consisting of yolky endoderm cells. yolk sac: Bag-like extraembryonic membrane extending from the midgut. yolky endoderm: Large cells fil led with yolk such as those in the floor of the amphibian midgut. ltona pellucida: A surface coat exterior to the pla$ma membrane of mammalian 'W·