Axonal and dendritic arborization of an intracellularly labeled chandelier cell in the CA1 region of rat hippocampus

SummaryDuring the course of an in vivo intracellular labeling study, a chandelier (axo-axonic) cell was completely filled with biocytin in the CA1 region of the hippocampus. Chandelier cells are known to provide GABAergic terminals exclusively to the axon initial segment of pyramidal cells. The lateral extent and laminar distribution of the dendritic arborization of the chandelier cell was very similar to that of pyramidal cells; the numerous basal and apical dendrites reached the ventricular surface and the hippocampal fissure, respectively. The dendrites, however, had very few spines. The neuron had an asymmetric axonal arbor occupying an elliptical area of 600 by 850 μm in the pyramidal cell layer and stratum oriens, with over three-quarters of the axon projecting to the fimbrial side of the neuron. Counting all clusters of terminals, representing individually innervated axon initial segments, the chandelier cell was estimated to contact 1214 pyramidal cells, a number that exceeds previous estimations, based on Golgi studies, by several-fold. The findings support the view that chandelier cells may control the threshold and/or synchronize large populations of principal cells.

[1]  P. Somogyi,et al.  Glutamate decarboxylase‐immunoreactive terminals of Golgi‐impregnated axoaxonic cells and of presumed basket cells in synaptic contact with pyramidal neurons of the cat's visual cortex , 1983, The Journal of comparative neurology.

[2]  T. Kosaka Axon initial segments of the granule cell in the rat dentate gyrus: synaptic contacts on bundles of axon initial segments , 1983, Brain Research.

[3]  Y. Mizoshita,et al.  THE NEW TYPE , 1937, 1997 IEEE International Magnetics Conference (INTERMAG'97).

[4]  F. Dudek,et al.  Electrophysiological evidence from glutamate microapplications for local excitatory circuits in the CA1 area of rat hippocampal slices. , 1988, Journal of neurophysiology.

[5]  Yasuo Kawaguchi,et al.  Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection , 1987, Brain Research.

[6]  F. F. Weight,et al.  Perforant pathway-evoked long-term potentiation of CA1 neurons in the hippocampal slice preparation , 1985, Brain Research.

[7]  M. Yeckel,et al.  Feedforward excitation of the hippocampus by afferents from the entorhinal cortex: redefinition of the role of the trisynaptic pathway. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[8]  F. F. Weight,et al.  Perforant pathway activation of hippocampal CA1 stratum pyramidale neurons: Electrophysiological evidence for a direct pathway , 1982, Brain Research.

[9]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[10]  O. Steward,et al.  Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat , 1976, The Journal of comparative neurology.

[11]  T. Freund,et al.  GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus , 1988, Nature.

[12]  M. Frotscher,et al.  A GABAergic axo-axonic cell in the fascia dentata controls the main excitatory hippocampal pathway , 1989, Brain Research.

[13]  C. Wilson,et al.  Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. , 1989, Journal of neurophysiology.

[14]  T. Kosaka The axon initial segment as a synaptic site: Ultrastructure and synaptology of the initial segment of the pyramidal cell in the rat hippocampus (CA3 region) , 1980, Journal of neurocytology.

[15]  P. Somogyi,et al.  A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells , 1983, Brain Research.

[16]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[17]  Kevan A. C. Martin,et al.  Control of Neuronal Output by Inhibition at the Axon Initial Segment , 1990, Neural Computation.

[18]  M. Frotscher,et al.  Axo‐axonic chandelier cells in the rat fascia dentata: Golgi‐electron microscopy and immunocytochemical studies , 1990, The Journal of comparative neurology.

[19]  P. Andersen Organization of Hippocampal Neurons and Their Interconnections , 1975 .

[20]  P. Schwartzkroin,et al.  Axonal ramifications of hippocampal Ca1 pyramidal cells , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  A. Cowey,et al.  The axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey , 1982, Neuroscience.

[22]  J. E. Vaughn,et al.  Immunocytochemical localization of GABAergic neurones at the electron microscopical level , 1981, The Histochemical Journal.

[23]  M. Arbib,et al.  Conceptual models of neural organization. , 1974, Neurosciences Research Program bulletin.

[24]  G. Buzsáki Feed-forward inhibition in the hippocampal formation , 1984, Progress in Neurobiology.

[25]  W. Cowan,et al.  On the numbers of neurons on fields CA1 and CA3 of the hippocampus of Sprague-Dawley and Wistar rats , 1987, Brain Research.

[26]  P. Somogyi,et al.  Identified axo-axonic cells are immunoreactive for GABA in the hippocampus visual cortex of the cat , 1985, Brain Research.