Summary
Parvalbumin-immunoreactive structures in the fascia dentata and Ammon's horn of the adult human brain were studied using the avidin-biotin-peroxidase technique. Thin fibres (probably axons) were found to form dense networks throughout the cellular layers. Parvalbumin immunoreactivity is observed in even distal portions of nerve cell processes. The excellent quality of the immunoreaction renders the distinction of a large number of possible neuronal types. All parvalbumin-immunoreactive neurons belong to the class of non-granule cells in the fascia dentata and non-pyramidal neurons in Ammon's horn. The fascia dentata harbours four types of neurons in the molecular layer, one type within the granule cell layer and four types in the plexi-form layer. The frequently described basket cells are contained in the group of immunoreactive non-granule cells in the plexiform layer. In field CA4 two neuronal types can be distinguished. Field CA3 reveals a slender cell type in the stratum radiatum, three types in the pyramidal cell layer and three types in the stratum oriens. In field CA2 three neuronal types can be differentiated in the stratum pyramidale. The extended field CA1 is endowed with two types of nerve cells within the stratum moleculare, two types in the stratum radiatum, five neuronal types in the stratum pyramidale, and one spindle-shaped type in the stratum oriens. The morphological features of parvalbumin-immunoreactive neuronal types in the adult human brain are compared with those found in Golgi-studies of mostly young animals or in labelling experiments. This study serves as a basis for further analyzes involving specific diseases such as Alzheimer's disease or epilepsy, where it needs to be clarified to which extent certain neuronal types are afflicted.
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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
Amaral DG, Campbell MJ (1986) Transmitter systems in the primate dentate gyrus. Hum Neurobiol 5:169–180
Amaral DG, Woodward DJ (1977) A hippocampal interneuron observed in the inferior region. Brain Res 124:225–236
Amaral DG, Insausti R, Cowan MW (1984) The commissural connections of the monkey hippocampal formation. J Comp Neurol 224:307–336
Anderson KJ, Maley BE, Scheff SW (1986) Immunocytochemical localization of γ-aminobutyric acid in the rat hippocampal formation. Neurosci Lett 69:7–12
Babb TL, Pretorius JK, Kupfer WR, Brown WJ (1988) Distribution of glutamate-decarboxylase-immunoreactive neurons and synapses in the rat and monkey hippocampus: light and electron microscopy. J Comp Neurol 278:121–138
Bakst I, Morrison JH, Amaral DG (1985) The distribution of somatostatin-like immunoreactivity in the monkey hippocampal formation. J Comp Neurol 236:423–442
Berchtold MW, Celio MR, Heizmann CW (1985) Parvalbumin in human brain. J Neurochem 45:235–239
Braak H (1974) On the structure of human archicortex. I. The cornu ammonis. A Golgi and pigmentarchitectonic study. Cell Tissue Res 152:349–383
Braak H (1980) Architectonics of the human telencephalic cortex. In: Braitenberg V, Barlow HB, Bizzi E, Florey E, Grüsser OJ, Van der Loos H (eds) Studies of brain function, vol 4. Springer, Berlin Heidelberg New York, pp 1–147
Braak E, Olbrich HG, Braak H, Wieser HG, Oertel WH (1986) Glutamic acid decarboxylase immunoreactivity in sector CA1 of the human Ammon's horn. Anat Embryol 175:15–23
Braak H, Braak E, Ohm T, Bohl J (1988) Silver impregnation of Alzheimer's neurofibrillary changes counterstained for basophilic material and lipofuscin pigment. Stain Technol 63:197–200
Braak E, Strotkamp B, Braak H (1989) Identification of non-pyramidal cells in the adult human hippocampus by means of antiparvalbumin immunostaining (abstract). Soc Neurosci 15:1249
Celio MR (1986) Parvalbumin in most γ-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231:995–997
Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35:375–475
Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300–302
Celio MR, Baier W, Schärer L, De Viragh PA, Gerday C (1988) Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9:81–86
Chan-Palay V (1987) Somatostatin immunoreactive neurons in the human hippocampus and cortex shown by immunogold/silver intensification on Vibratome sections: coexistence with neuropeptide Y neurons, and effects in Alzheimer-type dementia. J Comp Neurol 260:201–223
Chan-Palay V, Köhler C, Haesler U, Lang W, Yasargil G (1986) Distribution of neurons and axons immunoreactive with antisera against neuropeptide Y in the normal human hippocampus. J Comp Neurol 248:360–375
Demeter S, Rosene DL, Van Hoesen GW (1985) Interhemispheric pathways of the hippocampal formation, presubiculum, entorhinal and posterior parahippocampal cortices in the rhesus monkey: the structure and organization of the hippocampal commissures. J Comp Neurol 233:30–47
Freund TF (1989) GA BAergic septohippocampal neurons contain parvalbumin. Brain Res 478:375–381
Gamrani H, Onteniente B, Seguela P, Geffard M, Calas A (1986) Gamma-aminobutyric acid-immunoreactivity in the rat hippocampus. A light and electron microscopic study with anti-GABA antibodies. Brain Res 364:30–38
Heizmann CW, Berchtold MW (1987) Expression of parvalbumin and other Ca2+-binding proteins in normal and tumor cells: a topical review. Cell Calcium 8:1–41
Heizmann CW, Hunziker W (1990) Intracellular calcium-binding molecules. In: Bronner F (ed) Intracellular calcium regulation. Liss, New York, pp 211–248
Holm IE, Geneser FA, Zimmer J, Baimbridge KG (1990) Immunocytochemical demonstration of the calcium-binding proteins calbindin-D 28k and parvalbumin in the subiculum, hippocampus and dentate area of the domestic pig. Exp Brain Res 72:347–362
Kageyama GH, Wong-Riley MTT (1982) Histochemical localization of cytochrome oxidase in the hippocampus: correlation with specific neuronal types and afferent pathways. Neuroscience 7:2337–2361
Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347–362
Kawaguchi Y, Hama K (1987a) Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection. Brain Res 411:190–195
Kawaguchi Y, Hama K (1987b) Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats. Brain Res 425:351–355
Kawaguchi Y, Hama K (1988) Physiological heterogeneity of non-pyramidal cells in rat hippocampal CA1 region. Exp Brain Res 72:494–502
Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K (1987) Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res 416:369–374
Knowles WD, Schwartzkorin PA (1981) Local circuit synaptic interactions in hippocampal brain slices. J Neurosci 1:318–322
Kölliker A (1896) Handbuch der Gewebelehre des Menschen, vol 2. Nervensystem des Menschen und der Thiere, 6th edn. Engelmann, Leipzig
Kosaka T, Katsumaru H, Hama K, Wu JY, 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, Heizmann CW, Barnstable CJ (1989) Monoclonal antibody VC1.1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp Brain Res 78:43–50
Kunkel DD, Lacaille JC, Schwartzkroin PA (1988) Ultrastructure of stratum lacunosum-moleculare interneurons of hippocampal CA1 region. Synapse 2:382–394
Lacaille JC, Schwartzkroin PA (1988) Stratum lacunosum-moleculare interneurons of hippocampal CA1 region. I. Intercellular response characteristics, synaptic responses, and morphology. J Neurosci 8:1400–1410
Lacaille JC, Mueller AL, Kunkel DD, Schwartzkroin PA (1987) Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J Neurosci 7:1979–1993
Lewis DA, Lund JS (1990) Heterogeneity of chandelier neurons in monkey neocortex: corticotropin-releasing factor- and parvalbumin-immunoreactive populations. J Comp Neurol 293:599–615
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 46:113–176
Lotstra F, Vanderhaeghen JJ (1987) Distribution of immunoreactive cholecystokinin in the human hippocampus. Peptides 8:911–920
Lotstra F, Schiffmann SN, Vanderhaeghen JJ (1989a) Neuropeptide Y-containing neurons in the human infant hippocampus. Brain Res 478:211–226
Lotstra F, Schiffmann SN, Mailleux P, Vierendeels G, Vanderhaeghen JJ (1989b) High concentration of somatostatin-14 neurones in the infant human hippocampus. Neurochem Int 14:153–158
Nitsch R, Soriano E, Frotscher M (1990) The parvalbumin-containing non-pyramidal neurons in the rat hippocampus. Anat Embryol 181:413–425
Ohm TG, Müller H, Ulfig N, Braak E (1990) Glutamic-acid-decarboxylase-and parvalbumin-like-immunoreactive structures in the olfactory bulb of the human adult. J Comp Neurol 291:1–8
Peters A (1984) Chandelier cells. In: Peters A, Jones EG (eds) Cerebral Cortex, vol 1 Cellular components of the cerebral cortex. Plenum Press, New York, pp 361–380
Peters A, Harriman KM (1988) Enigmatic bipolar cell of rat visual cortex. J Comp Neurol 267:409–432
Ramón y Cajal S (1909/11) Histologie du Système Nerveux de l'Homme et des Vertébrés (translated by Azoulay L). Maloine, Paris
Ribak CE, Anderson L (1980) Ultrastructure of the pyramidal basket cells in the dentate gyrus of the rat. J Comp Neurol 192:903–916
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 (1988) A Golgi-electron microscopic study of fusiform neurons in the hilar region of the dentate gyrus. J Comp Neurol 271:67–78
Rosene DL, Van Hoesen GW (1987) The hippocampal formation of the primate brain. In: Jones EG, Peters A (eds) Cerebral cortex, vol 6. Further aspects of cortical function, including hippocampus. Plenum Press, New York London, pp 345–456
Scharfman HE, Schwartzkroin PA (1988) Electrophysiology of morphologically identified mossy cells of the dentate hilus recorded in guinea pig hippocampal slices. J Neurosci 8:3812–3821
Schwartzkroin PA, Kunkel DD (1985) Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol 232:205–218
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
Shinoda K, Tohyama M, Shiotani Y (1987) Hippocampofugal γ-amino-butyric acid (GABA)-containing neuron system in the rat: a study using a double-labeling method that combines retrograde tracing and immunocytochemistry. Brain Res 409:181–186
Sloviter RS (1989) Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of the hippocampal neurons to seizure activity. J Comp Neurol 280:183–196
Somogyi P, Takagi H (1982) A note of the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neuroscience 7:1779–1783
Somogyi P, Nunzi MG, Gorio A, Smith AD (1983a) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259:137–142
Somogyi P, Smith AD, Nunzi MG, Gorio A, Takagi H, Wu JY (1983b) 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
Somogyi P, Freund TF, Hodgson AJ, Somogyi J, Beroukas D, Chubb IW (1985) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res 332:143:149
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
Stephan H (1975) Allocortex. In: Bargmann W (ed) Handbuch der mikroskopischen Anatomie des Menschen, vol 4/9. Springer, Berlin Heidelberg New York, pp 1–998
Stephan H (1983) Evolutionary trends in limbic structures. Neurosci Behav Rev 7:367–374
Stephan H, Manolescu J (1980) Comparative investigations on hippocampus in insectivores and primates. Z Mikrosk Anat Forsch 94:1025–1050
Taber KH, Lin CT, Liu JW, Thalmann RH, Wu JY (1986) Taurine in hippocampus: localization and postsynaptic action. Brain Res 386:113–121
Wieser HG (1986) Selective amygdalohippocampectomy: indications, investigative technique and results. In: Symon L (ed) Adv Tech Stand Neurosurg 13:39–133
Wong-Riley MTT (1989) Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101
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Braak, E., Strotkamp, B. & Braak, H. Parvalbumin-immunoreactive structures in the hippocampus of the human adult. Cell Tissue Res 264, 33–48 (1991). https://doi.org/10.1007/BF00305720
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DOI: https://doi.org/10.1007/BF00305720