Summary
Recent studies have indicated that hippocampal basket cells in both the dentate gyrus and Ammon's horn develop their somal and dendritic features during the first two postnatal weeks in rats. Their axon terminals form exclusively symmetric synapses that are found as early as 5 postnatal days in both regions. The present study used Golgi-electron microscopic material from 10 and 16 day old rats to demonstrate that the axon terminals of basket cells form synapses not only with somata, dendrites, and dendritic spines as reported for adult material but also with axon initial segments. However, the terminals forming synapses with axon initial segments and dendritic spines represent only a minor portion of the total number of basket cell terminals. Quantitative results indicate that 36–62% of the total number of these terminals form axosomatic synapses and 32–50% form axodendritic synapses depending on the analyzed cell. These data indicate that hippocampal basket cells have an axonal distribution similar to that found for cortical basket cells.
Similar content being viewed by others
References
Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851–914
Andersen P, Eccles JC, Løyning Y (1964a) Location of postsynaptic inhibitory synapses on hippocampal pyramids. J Neurophysiol 27:592–607
Andersen P, Eccles JC, Løyning Y (1964b) Pathway of postsynaptic inhibition in the hippocampus. J Neurophysiol 27:608–619
Blackstad TW, Flood PR (1963) Ultrastructure or hippocampal axosomatic synapses. Nature 198:542–543
De Felipe J, Hendry SHC, Jones EG (1989) Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc Natl Acad Sci USA 86:2093–2097
Fairén A, Peters A, Saldanha J (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J Neurocytol 6:311–337
Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173
Frotscher M, Zimmer J (1983) Commissural fibers terminate on nonpyramidal neurons in the guinea pig hippocampus: a combined Golgi/EM degeneration study. Brain Res 265:289–293
Hendry SHC, Jones EG, Emson PC, Lawson DEM, Heizmann CW, Streit P (1989) Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 76:467–472
Jones EG (1975) Varities and distribution of non-pyramidal cells in the somatic sensory cortex of the squirrel monkey. J Comp Neurol 160:205–268
Jones EG, Hendry SHC (1984) Basket cells. In: Peters A, Jones EG (eds) Cerebral cortex, Vol 1. Cellular components of the cerebral cortex. Plenum, New York London, pp 309–336
Kosaka T, Hama K, Wu J-Y (1984) GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus. Brain Res 293:353–359
Kosaka T, Katsumaru H, Hama K, Wu J-Y, Heizmann CW (1987) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119–130
Kosaka T, Wu J-Y, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388–398
Kunkel DD, Hendrickson AE, Wu J-Y, Schwartzkroin PA (1986) Glutamic acid decarboxylase (GAD) immunocytochemistry of developing rabbit hippocampus. J Neurosci 6:541–552
Lang U, Frotscher M (1990) Postnatal development of non-pyramidal neurons in the rat hippocampus (areas CA 1 and CA 3): a combined Golgi-electron microscope study. Anat Embryol (in press)
Léránth C, Frotscher M (1987) Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33–47
Lorente de Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46:113–177
Lübbers K, Frotscher M (1987) Fine structure and synaptic connections of identified neurons in the rat fascia dentata. Anat Embryol 177:1–14
Ramón y Cajal S (1911) Histologie du système nerveux de l'homme et des vertébrés, Tome II. Maloine, Paris
Ribak CE, Nitsch R, Seress L (1990) Proportion of parvalbumin-positive basket cells in the GABAergic innervation of pyramidal and granule cells of the rat hippocampal formation. J Comp Neurol (in press)
Ribak CE, Seress L (1983) Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J Neurocytol 12:577–597
Ribak CE, Seress L, Peterson GM, Seroogy KB, Fallon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. J Neurosci 6:3492–3498
Ribak CE, Vaughn JE, Barber RP (1981) Immunocytochemical localization of GABAergic neurones at the electron microscopical level. Histochem J 13:555–582
Ribak CE, Vaughn JE, Saito K (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res 140:315–332
Seress L, Frotscher M, Ribak CE (1989) Local circuit neurons in both the dentate gyrus and Ammon's horn establish synaptic connections with principal neurons in five day old rats: a morphological basis for inhibition in early development. Exp Brain Res 78:1–9
Seress L, Pokorny J (1981) Structure of the granular layer of the rat dentate gyrus: a light microscopic and Golgi study. J Anat 133:181–195
Seress L, Ribak CE (1983) GABAergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 50:173–182
Seress L, Ribak CE (1984) Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feed-forward inhibition. J Neurocytol 13:215–225
Seress L, Ribak CE (1985) A combined Golgi-electron microscopic study of non-pyramidal neurons in the CA 1 area of the hippocampus. J Neurocytol 14:717–730
Seress L, Ribak CE (1990) Postnatal development of the light and electron microscopic features of basket cells in the hippocampal dentate gyrus of the rat. Anat Embryol (in press)
Sloviter RS (1989) Calcium-binding protein (Calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183–196
Sloviter RS, Nilaver G (1987) Immunocytochemical localization of GABA-, cholecystokinin-, vasoactive intestinal polypeptide-, and somatostatin-like immunoreactivity in the area dentata and hippocampus of the rat. J Comp Neurol 256:42–60
Somogyi P (1977) A specific axo-axonal neuron in the visual cortex of the rat. Brain Res 136:345–350
Somogyi P, Smith AD, Nunzi MG, Gorio A, Takagi H, Wu J-Y (1983) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons. J Neurosci 3:1450–1468
Soriano E, Frotscher M (1989) A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway. Brain Res 503:170–174
Soriano E, Nitsch R, Frotscher M (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-electron microscopy and immunocytochemical studies. J Comp Neurol 293:1–25
Szentágothai J, Arbib M (1974) Conceptual models of neural organization. Neurosci Res Program Bull 12:307–510
Zecevic N, Bourgeois J-P, Rakic P (1989) Changes in synaptic density in motor cortex of rhesus monkey during fetal and postnatal life. Dev Brain Res 50:11–32
Zipp F, Nitsch R, Soriano E, Frotscher M (1989) Entorhinal fibers form synaptic contacts on parvalbumin-immunoreactive neurons in the rat fascia dentata. Brain Res 495:161–166
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Seress, L., Ribak, C.E. The synaptic connections of basket cell axons in the developing rat hippocampal formation. Exp Brain Res 81, 500–508 (1990). https://doi.org/10.1007/BF02423498
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02423498