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Development of the lateral amygdaloid nucleus in the human fetus: transient presence of discrete cytoarchitectonic units

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The cytoarchitectonic development of the lateral amygdaloid nucleus has been studied on Nissl-stained sections through brains of human fetuses ranging between 11 to 24 weeks of gestation. The first sign of cytoarchitectonic inhomogeneity of the lateral amygdaloid nucleus is the appearance of 2–3 ovoid cell clusters around 12 weeks of gestation. Between 12.5–16 weeks of gestation, the ventral part of the lateral amygdaloid nucleus contains 7–11 columnar cell clusters separated by “septa” of lower cell-packing density. These columnar clusters, stretching in the rostrocaudal direction, appear on cross-section as ovoid structures elongated in the ventrodorsal direction. In subsequent development (16–24 weeks of gestation) this distinct columnar appearance becomes less obvious, owing to the disappearance of “septa” along the dorsal edges of cellular clusters. This process begins first in the medial part of the columnar field. As a result, the cytoarchitectonic units gradually fuse into a homogeneous grey mass. However, the ventral part of the columnar field retains an undulated appearance throughout late gestation, showing multiple indentations as a sign of former cytoarchitectonic inhomogeneities. In conclusion, the fetal lateral amygdaloid nucleus contains a number of cytoarchitectonic “moduli” which could serve as a new parameter for an estimation of histogenetic maturity of the human amygdala. This transient cytoarchitectonic inhomogeneity could be a sign of the temporary predominance of one characteristic afferent-efferent system during a given developmental stage. Alternatively, it could reflect a clustered type of neurogenesis.

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  1. Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the Cynomolgus monkey. J Comp Neurol 222:56–68

  2. Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347–368

  3. Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591

  4. Amaral DG, Veazey RB, Cowan WM (1982) Some observations on hypothalamo-amygdaloid connections in the monkey. Brain Res 252:13–27

  5. Avendano C, Price JL, Amaral DG (1983) Evidence for an amygdaloid projection to premotor cortex but not to motor cortex in the monkey. Brain Res 264:111–117

  6. Bayer SA (1980) Quantitative3H-thymidine radiographic analyses of neurogenesis in the rat amygdala. J Comp Neurol 194:845–875

  7. Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell labelling with horseradish peroxidase. Brain Res 152:249–264

  8. Belford GR, Killackey HP (1979) The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 188:63–74

  9. Braak H, Braak E (1983) Neuronal types in teh basolateral amygdaloid nuclei of man. Brain Res Bull 11:349–365

  10. Brand S, Rakic P (1979) Genesis of the primate neostriatum:3H-thymidine autoradiographic analysis of the time of neuron origin in the rhesus monkey. Neuroscience 4:467–478

  11. Fallon JH, Koziell DA, Moore RY (1978) Catecholamine innervation of the basal forebrain: II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 180:509–532

  12. Goldman PS, Nauta WHJ (1977) Columnar distribution of corticocortical fibres in the frontal association, limbic, and motor cortex of the developing rhesus monkey. Brain Res 122:393–413

  13. Goldman-Rakic PS (1981) Prenatal formation of cortical input and development of cytoarchitectonic compartments in the neostriatum of the rhesus monkey. J Neurosci 1:721–735

  14. Graybiel AM, Ragsdale CW Jr (1980) Clumping of acetylcholinesterase activity in the developing striatum of the human fetus and young infant. Proc Natl Acad Sci USA 77:1214–1218

  15. Graybiel AM, Pickel VM, Joh TH, Reis DJ, Ragsdale CW (1981) Direct demonstration of a correspondence between the dopamine islands and acetylcholinesterase patches in the developing striatum. Proc Natl Acad Sci USA 78:5871–5875

  16. Hall E (1972) Some aspects of the structural organization of the amygdala. In: Eleftheriou BE (ed) The neurobiology of the Amygdala. Plenum Press, New York, pp 95–121

  17. Herzog AG, Van Hoesen GW (1976) Temporal neocortical afferent connections to the amygdala in the rhesus monkey. Brain Res 115:57–69

  18. Hochstetter F (1919) Beiträge zur Entwicklungsgeschichte des menschlichen Gehirns, vol 1. Deuticke, Leipzig Wien

  19. Hopkins DA, Holstege G (1978) Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp Brain Res 32:529–547

  20. Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond [Biol] 278:377–409

  21. Humphrey T (1972) Development of the human amygdaloid complex. In: Eleftheriou BE (ed) The neurobiology of the Amygdala. Plenum Press, New York London, pp 21–80

  22. Ivy GO, Killackey HP (1982) Ephemeral cellular segmentation in the thalamus of the neonatal rat. Develop Brain Res 2:1–17

  23. Jacobson S, Trojanowski JQ (1975) Amygdaloid projections to prefrontal granular cortex in rhesus monkey demonstrated with horseradish peroxidase. Brain Res 100:132–139

  24. Jeanmonod D, Rice FL, Van der Loos H (1981) Mouse somatosensory cortex: Alterations in the barrelfield following receptor injury at different early postnatal ages. Neuroscience 2: 1503–1535

  25. Johnston JB (1923) Further contributions to the study of the evolution of the forebrain. J Comp Neurol 35:337–481

  26. Jones EG, Burton H (1976) Projection from the medial pulvinar to the amygdala in primates. Brain Res 104:142–147

  27. Kelley AE, Domesick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat — an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7:615–630

  28. Kelović Z, Kostović I (1981) Banding pattern in human entorhinal cortex revealed by acetylcholinesterase histochemistry. Anat Rec 199:135A-136A

  29. Klinger J, Gloor P (1960) The connections of the amygdala and of the anterior temporal cortex in the human brain. J Comp Neurol 115:333–369

  30. Kostović I (1979) Columnar distribution of acetylcholinesterase staining in the frontal cortex of the human fetus. Neurosci Lett [Suppl] 3:22

  31. Kostović I (1983) Transient correspondence between the cytoarchitectonic compartments and the pattern of histochemical heterogeneity in the putamen of the human fetus and newborn infant. Neurosci Lett [Suppl] 14:S207

  32. Kostović I, Goldman-Rakic PS (1983) Transient cholinesterase staining in the mediodorsal nucleus of the thalamus and its connections in the developing human and monkey brain. J Comp Neurol 219:431–447

  33. Kostović I, Krmpotić-Nemanić J (1976) Early prenatal ontogenesis of the neuronal connections in the interhemispheric cortex of the human gyrus cinguli. Verh Anat Ges 70:S305-S316

  34. Kostović I, Rakic P (1984) Development of prestriate visual projections in the monkey and human fetal cerebrum revealed by transient cholinesterase staining. J Neurosci 4:25–42

  35. Krettek JE, Price JL (1977a) Projections from the amygdaloid complex to the cerebral cortex and thalamus in the rat and cat. J Comp Neurol 172:687–722

  36. Krettek JE, Price JL (1977b) Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and rat. J Comp Neurol 172:723–752

  37. Macchi G (1951) Development of the olfactory centers in man. J Comp Neurol 95:245–305

  38. McConnel J, Angevine J (1983) Time of origin in the amygdaloid complex of the mouse. Brain Res 272:150–156

  39. Mehler WR (1980) Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190:733–762

  40. Molliver ME, Kostović I, Van der Loos H (1973) The development of synapses in cerebral cortex of the human fetuses. Brain Res 50:403–407

  41. Mufson EJ, Mesulam MM, Pandya DN (1981) Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 6:1231–1248

  42. Nauta WJH (1961) Fibre degeneration following lesions of the amygdaloid complex in the monkey. J Anat 95:515–531

  43. Nikolić I, Kostović I, Marinković R (1982) Development of the lateral amygdaloid nucleus in human fetus: Presence of column-like morphological units. Neuroscience [Suppl]: The brain in health and disease:S158 (abstr)

  44. Oliver G, Pineau H (1961) Horizons de Streeter et age embryonnaire. Bull Assoc Anat (Nancy) 47e:573–576

  45. Porrino LJ, Crane AM, Goldman-Rakic PS (1981) Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkey. J Comp Neurol 198:121–136

  46. Price JL, Amaral DG (1982) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259

  47. Rakic P (1977) Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond [Biol] 278:245–260

  48. Russchen FT (1982) Amygdaloid projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159–179

  49. Stephan H (1975) Allocortex. In: Bargmann W (ed) Handbuch der mikroskopischen Anatomie des Menschen, vol IV/9. Springer, Berlin Heidelberg New York

  50. Svendsen CN, Bird ED (1985) Acetylcholinesterase staining of the human amygdala. Neurosci Lett 54:313–318

  51. Tennyson VM, Barrett RE, Cohen G, Cote L, Heikkila R, Mytilineou C (1972) The developing neostriatum of the rabbit: Correlation of fluorescence histochemistry, electron microscopy, endogenous dopamine levels, and (3H) dopamine uptake. Brain Res 46:251–285

  52. Turner BH, Mishkin M, Knapp M (1980) Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J Comp Neurol 191:515–543

  53. Van Hoesen GW (1981) The different distribution, diversity and sprouting of cortical projections to the amygdala in the rhesus monkey. In: Ben Ari Y (ed) The amygdaloid complex. Elsevier/North Holland, New York, pp 77–90

  54. Wakefield CL, Levine MS (1985) Early postnatal development of basolateral amygdala in kitten: A golgi morphometric analysis. Brain Res Bull 14:159–167

  55. Woolf NJ, Butcher LL (1982) Cholinergic projections to the basolateral amygdala: A combined Evans blue and acetylcholinesterase analysis. Brain Res Bull 8:751–763

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Correspondence to Ivica Kostović.

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Nikolić, I., Kostović, I. Development of the lateral amygdaloid nucleus in the human fetus: transient presence of discrete cytoarchitectonic units. Anat Embryol 174, 355–360 (1986). https://doi.org/10.1007/BF00698785

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Key words

  • Lateral amygdaloid nucleus
  • Ontogenesis
  • Man
  • Cytoarchitectonics