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HANDBOOK O FCHEMICAL NEUROANATOMY
Volume 10:
ONTOGENY OFTRANSMITTERS ANDPEPTIDES IN THE CNS
A . BJÖRKLUND
T . HÖKFELT
M . TOHYAMA
List of contributors
vPreface i x
I . THE EARLY STAGES OF NERVOUS SYSTEM DEVELOPMENT :NEUROGENESIS AND NEURONAL MIGRATION - J . ALTMA N
1. Introduction
12. The loci of neuron production
32 .1 . The primary neuroepithelium
32 .2 . Compartmentation in the neuroepithelium
32 .3 . Mosaicism in the neuroepithelium
82 .4 . Secondary germinal matrices
83. The chronology of neuron production
1 03 .1 . Precision in the temporal order of neurogenesis
1 03 .2 . Sequential order in neurogenesis
1 04. Neuronal migration and pauses in sojourn zones
1 54 .1 . Translocation and different patterns of migration
1 54 .1 .1 . Passive translocation and migration along a straight path
1 54 .1 .2 . Cell-sorting migration
1 54 .1 .3 . Migration along curved paths and over long distances
1 64 .1 .4 . Divergent and convergent migration
1 94 .2 . Sojourn zones in transitional cortex
2 14 .3 . The lateral cortical stream
2 35. Conclusion
2 76. Acknowledgments
2 77. List of abbreviations
2 78. References
2 9
II . DEVELOPMENT OF CENTRAL CHOLINERGIC NEURONS - K . SEMB A
1. Introduction
3 32. The whole brain
343. Basal forebrain
3 4
3 .1 . Time of origin
3 5
3 .2 . Onset of cholinergic phenotype expression and migration
3 5
3 .2 .1 . AChE histochemistry
3 5
3 .2 .2 . ChAT immunohistochemistry
40
3 .2 .3 . NGF-receptor immunohistochemistry
40
3 .3 . Cellular differentiation and maturation
4 1
3 .4 . Axonal outgrowth
4 1
3 .4 .1 . Septohippocampal projections
41
3 .4 .2 . Nucleus basalis magnocellularis-neocortical projections
423 .5 . Unsettled problems
444. Cerebral cortex
4 54 .1 . Hippocampus
4 54 .1 .1 . Neurochemistry
4 54 .1 .2 . Cholinergic interneurons
4 54 .1 .3 . Cholinergic receptors
4 54 .2. Neocortex
454 .2 .1 . Neurochemistry
4 54 .2 .2 . Cholinergic innervation of the visual cortex
464 .2 .3 . Transient expression of AChE in thalamocortical fibers
464 .2 .4 . Intrinsic neurons of the cortex
474 .2 .5 . Receptors
4 75. Caudate putamen
4 85 .1 . Neurochemistry
4 85 .2 . Time of origin
4 85 .3 . Expression of cholinergic phenotype and morphologica l
maturation
505 .4 . Receptor binding
506. Mesopontine tegmentum
5 27. Spinal cord
5 27 .1 . Time of origin
5 27 .2 . Cholinergic phenotype and cellular differentiation
5 48. Conclusions
5 49. Acknowledgments
5 610. References
5 6
III . DEVELOPMENT OF DOPAMINE-CONTAINING SYSTEMS IN TH ECNS - A . KALSBEEK, P . VOORN AND R.M . BUIJ S
1. Introduction
6 32. Visualization of dopamine
643. Development of the mesotelencephalic dopaminergic system
6 53 .1 . Cell groups in the ventral mesencephalon
6 63 .2 . The mesostriatal innervation
683 .3 . The mesocortical innervation
8 04. Development of hypothalamic-dopaminergic systems
945. Development of dopamine-containing structures in the brainstem
996. Development of other dopaminergic systems
10 17. Dopaminergic systems in the human fetus
10 58. Acknowledgments
1069. References
106
IV . IMMUNOCYTOCHEMICAL DISTRIBUTION OF AROMATI CL-AMINO ACID DECARBOXYLASE (AADC) IN RAT EMBRYO S
C.B. JAEGER AND G . TEITELMA N
1. Introduction
11 32. Localization of D groups in the brain
11 42 .1 . D groups in embryos at 15 days of gestation
11 42 .2 . D groups in embryos at 16 days of gestation (Figs . 3 and 4)
11 72 .3 . D groups in embryos at 19 days of gestation
11 93. Localization of D groups in the periphery
12 64. Summary and discussion
12 75. Acknowledgments
12 86. List of abbreviations
12 87. References
13 1
V. PHENYLETHANOLAMINE N-METHYLTRANSFERASE -THE ADRENALINE-SYNTHESIZING ENZYME - G .A. FOSTER
1. Introduction
13 32. Immunohistochemical analysis of prenatal PNMT-LI and TH-L I
ontogeny
13 43. Prenatal regulation of PNMT and TH expression
14 44. Neurochemical analysis of prenatal development of adrenergic neuron s
of the medulla oblongata
14 75. Immunohistochemical analysis of postnatal PNMT-LI development
15 06. Summary
15 17. List of abbreviations
15 18. References
154
VI . ONTOGENY OF HISTAMINE-IMMUNOREACTIVE NEURON SIN THE CNS - P . PANULA, A . KINNUNEN, M .S. AIRAKSINEN ,M . AHONEN, O . HÄPPOLA AND E . CASTRE N
1. Introduction
15 72. Biochemical analysis of histamine during ontogenesis
1582 .1 . Brain
15 82 .2 . Other tissues
16 13. Morphological analysis of developing histamine-containing systems i n
mammals
16 13 .1 . Tuberomammillary histaminergic neurons in rat brain
16 13 .2 . Transient histamine-immunoreactive neurons in the CNS
1623 .3 . Histamine-immunoreactive nerve fibers in the rat CNS
1683 .4 . Mast cells in the rat brain
1683 .5 . Histamine-immunoreactive neurons in the CNS of other species
1683 .6 . Pefipheral nervous system
17 13 .7 . Phylogenetic aspects
17 34. Conclusions
173
5. List of abbreviations
17 36. References
17 4
VII . POSTNATAL CHANGES OF GLUTAMINASE-LIK EIMMUNOREACTIVITY IN THE OLFACTORY BULB, THALAMUS ,CEREBRAL CORTEX AND CEREBELLUM OF THE RA T- T. KANEKO AND N. MIZUNO
1. Introduction
17 72. Materials and methods
17 83. Results
17 93 .1 . Olfactory bulb and pyriform cortex
17 93 .2 . Thalamus
17 93 .3 . Cerebral neocortex
18 53 .4 . Hippocampus and entorhinal cortex
18 53 .5 . Cerebellum and precerebellar nuclei
18 54. Discussion
19 15. Summary
19 26. Acknowledgment
19 37. References
19 3
VIII . DEVELOPMENT OF NEURONAL ELEMENTS WITH SUBSTANCEP-LIKE IMMUNOREACTIVITY IN THE CENTRAL NERVOUSSYSTEM - M . SAKANAK A
1. Introduction
19 7
2. Methodology
1993. Ontogeny of neuronal elements with SPI in the brain
1993 .1 . Rat brain
199
3 .1 .1 . General organization
199
3 .1 .2 . Development of SPI in specific brain regions
22 5
3 .2 . Mouse brain
23 5
3 .3 . Human brain
23 7
3 .4 . Rabbit brain
237
3 .5 . Xenopus embryonic brain
23 8
4. Development of SPI in the spinal cord and dorsal root ganglion
23 8
4 .1 . Rat
23 8
4 .2. Human
244
4 .3. Opossum
244
4 .4. Chicken
245
4 .5 . Xenopus
246
5. Factors that may affect the development of neuronal elements with SPI
246
6. Summary and conclusions
248
7. Acknowledgments
24 8
8. References
249
IX . ONTOGENETIC AND DIFFERENTIAL EXPRESSION OF TH EPREPROENKEPHALIN AND PREPRODYNORPHIN GENES IN TH ERAT BRAIN - Y . MORITA
I . Introduction
25 72. Methods
25 82 .1 . Animals and preparation of tissues
25 82 .2 . Probes
25 82 .3 . In-situ hybridization histochemistry (ISHH)
25 93. Results
25 93 .1 . Differential expression of PPE and PPD genes
25 93 .2 . Ontogenesis of the central PPE- and PPDergic systems
26 53 .2 .1 . Telencephalon
26 53 .2 .2 . Diencephalon
27 73 .2 .3 . Mesencephalon
28 13 .2 .4 . Rhombencephalon
28 33 .2 .5 . Cerebellum
28 74. Discussion
28 84 .1 . Differential expression of PPE and PPD genes
28 84 .2 . Ontogenesis of PPE and PPD gene expression
28 94 .3 . Possible functions of endogenous opioids in the developing brain
2905. Conclusions
29 16. Acknowledgments
29 17. List of abbreviations
29 18. References
29 2
X. ONTOGENY OF PRO-OPIOMELANOCORTIN (POMC)-DERIVE DPEPTIDES IN THE BRAIN AND PITUITARY Y .-Q. WANG, J .-S . LI ,
H.-M . LI AND M . TOHYAM A
1. Introduction
29 7
2. Ontogeny of POMC-derived peptides in the brain
29 72 .1 . ß-END-IR
298
2 .2 . ACTH-IR
3002 .3 . ;-MSH-IR
30 32 .4 . x-MSH-IR
31 0
2 .5 . General discussion
31 13. Ontogeny of POMC-derived peptides in the pituitary
31 3
3 .1 . z-MSH
31 33 .2 . ACTH-IR
31 4
3 .3 . ß-END and otherß-lipotropin (LPH)-related peptides
31 5
3 .4 . ;-MSH-IR
31 6
3 .5 . POMC gene expression
31 6
3 .6 . General discussion
31 7
4. Brain-pituitary interaction
31 9
5. Acknowledgment
31 9
6. References
319
XI. ONTOGENY OF CALCITONIN GENE-RELATED PEPTIDE (CGRP)- S . INAGAK I
1. Introduction
32 52. Ontogeny of CGRP-like immunoreactive (CGRPI) structures
32 62 .1 . Embryonic day 16 (E16)
32 62 .2 . Embryonic days 18-19 (E18-E19)
32 62 .3 . Embryonic day 20 (E20)
3262 .4 . Embryonic day 22 (E22)-postnatal day 1 (P 1)
3262 .5 . Postnatal days 2-7 (P2-P7)
3272 .6 . Postnatal days 8-14 (P8-P14)
33 82 .7 . Postnatal days 15-56 (P15-P56)
33 82 .8 . Cerebellum
3472 .9. Spinal cord
3473. General features of CGRP receptors
3503 .1 . Binding to brain homogenates
35 03 .2 . Binding to tissue sections
35 03 .3 . Autoradiography
35 14. Ontogeny of CGRP receptors
35 24 .1 . Receptor autoradiography
35 24 .1 .1 . Forebrain and diencephalon
35 74 .1 .2 . Posterior thalamus and midbrain
35 84 .1 .3 . Inferior colliculus and brainstem
35 85. Discussion
35 95 .1 . Development of CGRPI structures
35 95 .2 . Development of CGRP binding sites
36 15 .3 . Development of CGRP projections
36 15 .4 . Comparison of the localizations of CGRPI nerve fibers an d
CGRP binding sites
36 25 .5 . Comparison of the development of CGRP and other peptides
36 26. List of abbreviations
36 37. References
36 5
XII . ONTOGENY OF THE CENTRAL SOMATOSTATINERGIC SYSTE M- S. SHIOSAK A
1. Introduction
36 92. Biosynthesis of somatostatin
36 93. General profiles of the ontogeny of somatostatin-immunoreactiv e
structures in the brain
37 03 .1 . Prenatal ontogeny of somatostatinergic neurons
37 03 .2 . Postnatal ontogeny of somatostatinergic neurons
37 03 .3 . Prenatal ontogeny of somatostatinergic fibers
37 33 .4 . Postnatal ontogeny of somatostatinergic fibers
37 64. Ontogeny of somatostatinergic neurons in specific brain areas
37 64 .1 . Olfactory bulb
37 64 .2 . Cerebral cortex
37 64 .3 . Hippocampus
378
4 .4 .
Hypothalamus
38 04 .5 .
Piriform cortex, bed nucleus of the stria terminalis ,entopeduncular nucleus, and amygdala
38 24 .6 .
Other areas of the forebrain and upper brainstem
38 24 .7 .
Inferior and superior colliculus
38 24 .8 .
Lateral lemniscal nucleus including paralemniscal nucleus
38 54 .9 .
Periaqueductal gray, sphenoid nucleus, suprageniculate nucleus ,prepositus hypoglossal nucleus and its ventral extension (latera lto the FLM), trigeminal spinal tract nucleus (medial part), an dsolitary tract nucleus
39 14 .10 . Reticulotegmental nucleus of the pons, the dorsal and ventra l
cochlear nuclei, and marginal part of the trigeminal spinal trac tnucleus
39 14 .11 . Cerebellum
39 14 .12 . Spinal cord
39 14 .13 . Other areas in the lower brainstem
39 25. Ontogeny of somatostatin receptors
39 26. Conclusion
39 27. Acknowledgments
3928. List of abbreviations
39 39. References
39 5
XIII . ONTOGENY OF NEUROTENSIN IMMUNOREACTIVITY AND MRN AIN THE RAT CENTRAL NERVOUS SYSTEM - H . KIYAMA, M . SAT OAND P.C . EMSON
1. Introduction
39 92. General overview of neurotensin development in the CNS
400
3. Telencephalon
40 13 .1 . Olfactory system
40 1
3 .2 . Cerebral cortex and amygdaloid complex
40 3
3 .3 . Hippocampus
40 6
3 .4 . Basal ganglia and septum
40 8
4. Diencephalon
41 0
4 .1 . Thalamus
41 0
4 .2 . Hypothalamus
41 1
5. Mesencephalon and pons
41 6
6. Medulla
42 0
7. Spinal cord
42 0
8. Development of neurotensin binding sites
42 3
9. Conclusion
42 5
10. List of abbreviations
42 6
11. References
427
XIV . ONTOGENY OF CHOLECYSTOKININ IN THE CENTRAL NERVOU S
SYSTEM - H .-J . CHO AND K . JOO
1. Introduction
43 32. Materials and methods
4342 .1 . Experimental animals and tissue preparation
4342 .2 . Immunohistochemical procedure
4342 .3 . Preparation and specificity of antiserum
434
2 .4 . Terminology
43 53. Results
43 53 .1 . Ontogeny of the CCK-8 neuron system of forebrain and uppe r
brainstem
43 53 .1 .1 . Embryonic period
43 53 .1 .2 . Postnatal period
43 7
3 .2 . Ontogeny of the CCK-8 neuron system of the lower brainstem
44 53 .2 .1 . Embryonic period
44 53 .2 .2 . Postnatal period
44 54. Discussion
44 75. List of abbreviations
45 26. References
45 4
XV. VASOACTIVE INTESTINAL POLYPEPTIDE AND PEPTIDE HISTIDIN E
ISOLEUCINE - K . HARES AND G.A. FOSTER
1. Introduction
45 7
2. Radioimmunoassay
45 83. In-situ hybridization
4604. Immunohistochemistry
460
5. Development of PHI-LI and VIP-LI in the rat central nervous system
4605 .1 . Embryonic period
4605 .2 . Postnatal period
46 5
6. Summary
4697. Discussion
4698. List of abbreviations
47 1
9. References
47 3
XVI. DEVELOPMENT OF CORTICOTROPIN-RELEASING FACTOR I NRAT BRAIN - S . DAIKOKU AND S . HISANO
1. Introduction
47 72. Anatomical distribution of CRF immunoreactivity in adult animals
4773. An overview of developing CRF neuron systems in the brain
48 1
4. Materials and methods
4824 .1 . Ontogenetic development of CRF neuron systems in the rat brain 48 2
4 .1 .1 . Light microscopy
48 24 .1 .2 . Electron microscopy
48 34 .1 .3 . Immunostaining
483
4 .2 . Transplantation of the embryonal hypothalamus and cerebra lcortex
48 45. Results
48 55 .1 . Prenatal development
48 55 .2 . Postnatal development
49 15 .3 . Transplantation study of the brain primordium
50 56. Discussion
51 06 .1 . Ontogenetic appearance of CRF neurons in rat hypothalamus
51 06 .2 . CRF fiber terminalis in the external layer of the median eminence 51 26 .3 . The presence of predetermined CRF neurons
51 37. Summary
51 48. Acknowledgments
51 59. References
51 5
XVII . NEUROPEPTIDE Y - G .A . FOSTER AND P .L. WOODHAM S
1. Introduction
52 12. Methods
52 23. Prenatal development of NPY-LI
52 23 .1 . Day 13 of gestation
52 23 .2 . Day 14 of gestation
52 83 .3 . Day 15 of gestation
52 93 .4 . Day 16 of gestation
52 93 .5 . Day 17 of gestation
52 93 .6 . Day 18 of gestation
53 13 .7 . Day 19 of gestation
53 13 .8 . Day 20 of gestation
53 13 .9 . Day 21 of gestation
53 34. Postnatal development of NPY
53 35. Transient NPY-containing neurons
53 86. Co-localization of NPY and other neuropeptides/transmitters
53 97. Summary
54 18. List of abbreviations
54 19. References
544
XVIII . THE DEVELOPMENT OF VASOPRESSIN AND OXYTOCIN SYSTEM SIN THE BRAIN - R .M . BUIJS
I . Introduction
54 72. The adult VP and OT systems
5483. The magnocellular neurons of the PVN and SON
5483 .1 . The magnocellular VP system
5493 .1 .1 . Day 15 of gestation
5493 .1 .2 . Day 16 of gestation
5493 .1 .3 . Day 17 of gestation
5493 .1 .4 . Day 18 of gestation
55 13 .1 .5 . Day 19 of gestation
552
3 .1 .6 . Day 20 of gestation
55 23 .1 .7 . Day 21 of gestation
55 23 .1 .8 . Postnatal development
55 23 .2 . The magnocellular OT system
55 23 .3 . Development of magnocellular neurons in other mammals
5543 .4 . Functional development of the magnocellular system
5564. Parvocellular neurons of the PVN
55 74 .1 . VP-containing parvocellular PVN neurons
55 84 .2 . OT-containing parvocellular PVN neurons
55 84 .3 . Functional development of the parvocellular VP and OT PV N
neurons
55 95. VP neurons of the SCN
5606. Development of SCN functions
56 27. VP neurons of the BST and Arne
5647 .1 . Development of BST and Arne neuron functions
56 68. VP cells in the locus ceruleus
56 69. Acknowledgments
56 610. References
56 7
XIX . ONTOGENY OF GONADOTROPIN-RELEASING HORMONE -CONTAINING NEURONAL SYSTEMS IN MAMMALS - L . JENNE SAND M . SCHWANZEL-FUKUD A
1. Introduction
57 32. The nervus terminalis
57 43. Development of the opossum GnRH system
57 43 .1 . Three months postnatal
57 73 .2 . Hypothalamus and preoptic area
57 74. Development of the mouse GnRH system
57 84 .1 . Autoradiography
58 15. Development of the rat GnRH system
58 15 .1 . Embryonic day 17
58 15 .2 . Embryonic day 18
58 35 .3 . Embryonic day 19
58 35 .4 . Day of birth (P0)
58 56. Development of the guinea pig GnRH system
58 86 .1 . Embryonic day 30
58 86 .2 . Embryonic day 35
58 86 .3 . Embryonic days 40-45
59 16 .4 . Embryonic days 50-60
59 17. Development of the rhesus macaque GnRH system
59 18. Discussion
59 29. Acknowledgments
59 510. List of abbreviations
59 511. References
596
XX . GALANIN - A .R . SIZER AND G .A. FOSTE R
I . Introduction
59 92. Experimental procedures
6003. Results
60 13 .1 . Prenatal ages
60 13 .2 . Postnatal ages
60 13 .2 .1 .
Day 1
60 13 .2 .2 .
Day 2
60 13 .2 .3 .
Day 4
60 13 .2 .4 .
Day 7
60 13 .2 .5 .
Day 11
60 63 .2 .6 .
Day 14
60 63 .2 .7 .
Day 16
60 83 .2 .8 .
Day 22
60 93 .2 .9 .
Day 28
60 93 .2 .10 . Day 38
61 13 .2 .11 . Aged rats
61 13 .3 . Radioimmunoassay
61 14. Discussion
61 25. List of abbreviations
61 26. References
61 5
XXI . DEVELOPMENT OF THE SEROTONERGIC SYSTEM IN RAT AN DCHICK EMBRYOS -- J .A . WALLACE AND J .M. LAUDER
1. Introduction
61 92. Development of the serotonergic system in the rat
61 92 .1 . Cell bodies
61 92 .1 .1 . Brainstem
61 92 .1 .2 . Diencephalon
62 32 .1 .3 . Spinal cord
62 32 .2 . Axonal projections
62 52 .2 .1 . Ascending
62 52 .2 .2 . Descending
63 03. Development of the serotonergic system in the chick
63 03 .1 . Cell bodies
63 03 .1 .1 . Brainstem
6303 .1 .2 . Diencephalon
63 63 .1 .3 . Spinal cord
63 63 .2 . Axonal projections
63 93 .2 .1 . Ascending
63 93 .2 .2 . Descending
64 14. Discussion
6425. Acknowledgments
6436. References
644
XXII. AN OVERVIEW OF THE ONTOGENY OF NEUROTRANSMITTER SAND NEUROMODULATORS IN THE CENTRAL NERVOUS SYSTE M- M . TOHYAM A
1. General aspects of the development of neurotransmitters an dneuromodulators
64 72. Importance of receptors
64 83. What is the `trophic role of neuroactive substances'?
64 93 .1 . Is cell death the cause of the postnatal decrease of neuroactiv e
substances or their mRNAs?
64 93 .2 . Is it possible to reinitiate production of neuroactive substance s
after the cessation of synthesis during postnatal ontogeny?
64 94. Discrepancies between the distribution of a neuroactive substance and
its mRNA during ontogeny
6505. References
650
SUBJECT INDEX
651