Anatomy and Embryology

, Volume 174, Issue 3, pp 355–360 | Cite as

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

  • Ida Nikolić
  • Ivica Kostović


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.

Key words

Lateral amygdaloid nucleus Ontogenesis Man Cytoarchitectonics 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Aggleton JP, Mishkin M (1984) Projections of the amygdala to the thalamus in the Cynomolgus monkey. J Comp Neurol 222:56–68Google Scholar
  2. Aggleton JP, Burton MJ, Passingham RE (1980) Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 190:347–368Google Scholar
  3. Amaral DG, Cowan WM (1980) Subcortical afferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591Google Scholar
  4. Amaral DG, Veazey RB, Cowan WM (1982) Some observations on hypothalamo-amygdaloid connections in the monkey. Brain Res 252:13–27Google Scholar
  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 264:111–117Google Scholar
  6. Bayer SA (1980) Quantitative3H-thymidine radiographic analyses of neurogenesis in the rat amygdala. J Comp Neurol 194:845–875Google Scholar
  7. Beckstead RM (1978) Afferent connections of the entorhinal area in the rat as demonstrated by retrograde cell labelling with horseradish peroxidase. Brain Res 152:249–264Google Scholar
  8. Belford GR, Killackey HP (1979) The development of vibrissae representation in subcortical trigeminal centers of the neonatal rat. J Comp Neurol 188:63–74Google Scholar
  9. Braak H, Braak E (1983) Neuronal types in teh basolateral amygdaloid nuclei of man. Brain Res Bull 11:349–365Google Scholar
  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 4:467–478Google Scholar
  11. Fallon JH, Koziell DA, Moore RY (1978) Catecholamine innervation of the basal forebrain: II. Amygdala, suprarhinal cortex and entorhinal cortex. J Comp Neurol 180:509–532Google Scholar
  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 122:393–413Google Scholar
  13. Goldman-Rakic PS (1981) Prenatal formation of cortical input and development of cytoarchitectonic compartments in the neostriatum of the rhesus monkey. J Neurosci 1:721–735Google Scholar
  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 77:1214–1218Google Scholar
  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 78:5871–5875Google Scholar
  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 95–121Google Scholar
  17. Herzog AG, Van Hoesen GW (1976) Temporal neocortical afferent connections to the amygdala in the rhesus monkey. Brain Res 115:57–69Google Scholar
  18. Hochstetter F (1919) Beiträge zur Entwicklungsgeschichte des menschlichen Gehirns, vol 1. Deuticke, Leipzig WienGoogle Scholar
  19. Hopkins DA, Holstege G (1978) Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Exp Brain Res 32:529–547Google Scholar
  20. Hubel DH, Wiesel TN, LeVay S (1977) Plasticity of ocular dominance columns in monkey striate cortex. Philos Trans R Soc Lond [Biol] 278:377–409Google Scholar
  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 21–80Google Scholar
  22. Ivy GO, Killackey HP (1982) Ephemeral cellular segmentation in the thalamus of the neonatal rat. Develop Brain Res 2:1–17Google Scholar
  23. Jacobson S, Trojanowski JQ (1975) Amygdaloid projections to prefrontal granular cortex in rhesus monkey demonstrated with horseradish peroxidase. Brain Res 100:132–139Google Scholar
  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: 1503–1535Google Scholar
  25. Johnston JB (1923) Further contributions to the study of the evolution of the forebrain. J Comp Neurol 35:337–481Google Scholar
  26. Jones EG, Burton H (1976) Projection from the medial pulvinar to the amygdala in primates. Brain Res 104:142–147Google Scholar
  27. Kelley AE, Domesick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat — an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7:615–630Google Scholar
  28. Kelović Z, Kostović I (1981) Banding pattern in human entorhinal cortex revealed by acetylcholinesterase histochemistry. Anat Rec 199:135A-136AGoogle Scholar
  29. Klinger J, Gloor P (1960) The connections of the amygdala and of the anterior temporal cortex in the human brain. J Comp Neurol 115:333–369Google Scholar
  30. Kostović I (1979) Columnar distribution of acetylcholinesterase staining in the frontal cortex of the human fetus. Neurosci Lett [Suppl] 3:22Google Scholar
  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:S207Google Scholar
  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 219:431–447Google Scholar
  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-S316Google Scholar
  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 4:25–42Google Scholar
  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 172:687–722Google Scholar
  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 172:723–752Google Scholar
  37. Macchi G (1951) Development of the olfactory centers in man. J Comp Neurol 95:245–305Google Scholar
  38. McConnel J, Angevine J (1983) Time of origin in the amygdaloid complex of the mouse. Brain Res 272:150–156Google Scholar
  39. Mehler WR (1980) Subcortical afferent connections of the amygdala in the monkey. J Comp Neurol 190:733–762Google Scholar
  40. Molliver ME, Kostović I, Van der Loos H (1973) The development of synapses in cerebral cortex of the human fetuses. Brain Res 50:403–407Google Scholar
  41. Mufson EJ, Mesulam MM, Pandya DN (1981) Insular interconnections with the amygdala in the rhesus monkey. Neuroscience 6:1231–1248Google Scholar
  42. Nauta WJH (1961) Fibre degeneration following lesions of the amygdaloid complex in the monkey. J Anat 95:515–531Google Scholar
  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)Google Scholar
  44. Oliver G, Pineau H (1961) Horizons de Streeter et age embryonnaire. Bull Assoc Anat (Nancy) 47e:573–576Google Scholar
  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 198:121–136Google Scholar
  46. Price JL, Amaral DG (1982) An autoradiographic study of the projections of the central nucleus of the monkey amygdala. J Neurosci 1:1242–1259Google Scholar
  47. Rakic P (1977) Prenatal development of the visual system in rhesus monkey. Philos Trans R Soc Lond [Biol] 278:245–260Google Scholar
  48. Russchen FT (1982) Amygdaloid projections in the cat. I. Cortical afferent connections. A study with retrograde and anterograde tracing techniques. J Comp Neurol 206:159–179Google Scholar
  49. Stephan H (1975) Allocortex. In: Bargmann W (ed) Handbuch der mikroskopischen Anatomie des Menschen, vol IV/9. Springer, Berlin Heidelberg New YorkGoogle Scholar
  50. Svendsen CN, Bird ED (1985) Acetylcholinesterase staining of the human amygdala. Neurosci Lett 54:313–318Google Scholar
  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 46:251–285Google Scholar
  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 191:515–543Google Scholar
  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 77–90Google Scholar
  54. Wakefield CL, Levine MS (1985) Early postnatal development of basolateral amygdala in kitten: A golgi morphometric analysis. Brain Res Bull 14:159–167Google Scholar
  55. Woolf NJ, Butcher LL (1982) Cholinergic projections to the basolateral amygdala: A combined Evans blue and acetylcholinesterase analysis. Brain Res Bull 8:751–763Google Scholar

Copyright information

© Springer-Verlag 1986

Authors and Affiliations

  • Ida Nikolić
    • 1
    • 2
  • Ivica Kostović
    • 1
    • 2
  1. 1.Department of Anatomy, Medical FacultyUniversity of Novi Sad, 21000Novi Sad, ZagrebYugoslavia
  2. 2.Section of Neuroanatomy, Department of Anatomy, Medical FacultyUniversity of ZagrebZagrebYugoslavia

Personalised recommendations