Postsynaptic-gabaergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus

Intracellular recording and staining was applied to study non-pyramidal neurons in the guinea-pig hippocampus. To avoid accidental impalement of pyramidal or granule cells, two hippocampal regions known to be devoid of pyramidal or granule cells were chosen. In transverse and longitudinal slices, neurons of the deep hilar region (zone 4 of Amaral3), and in transverse slices, neurons of the stratum lacunosum-moleculare (CA3) were impaled. The intracellular staining with Lucifer Yellow revealed that of 20 neurons stained in these zones all were non-pyramidal neurons. Hilar neurons, situated just below the granular layer, differed from granule cells and CA3 neurons with respect to their action potential waveform and their current/voltage relationship. In contrast to granule cells, hilar neurons exhibited spontaneous bursts in the presence of bicuculline (25 microM). In all neurons impaled in the hilar region and the stratum lacunosum-moleculare (n = 42), inhibitory postsynaptic potentials could be elicited. These inhibitory postsynaptic potentials were blocked by bicuculline. In transverse slices, perforant path stimulation elicited inhibition preceding excitation in hilar neurons and excitation preceding inhibition in granule cells. Since non-pyramidal neurons are likely to be inhibitory neurons, our data suggest that GABAergic neurons in the hilus or in the stratum lacunosum-moleculare are controlled by inhibitory GABAergic synapses. This was verified by immunocytochemistry using antibodies against glutamate decarboxylase, the gamma-aminobutyric acid synthetizing enzyme. In both hippocampal regions studied, glutamate decarboxylase-positive synaptic terminals on glutamate decarboxylase-positive cells were observed. It is concluded that disinhibition is an important feature of information processing in the hippocampus, and that disinhibition is mediated by GABAergic synapses on GABAergic neurons.

[1]  D. Prince,et al.  A calcium-activated hyperpolarization follows repetitive firing in hippocampal neurons. , 1980, Journal of neurophysiology.

[2]  T. Lømo,et al.  Participation of inhibitory and excitatory interneurones in the control of hippocampal cortical output. , 1969, UCLA forum in medical sciences.

[3]  P. Schwartzkroin,et al.  Further characteristics of hippocampal CA1 cells in vitro , 1977, Brain Research.

[4]  J. E. Vaughn,et al.  Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport , 1978, Brain Research.

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

[6]  T. H. Brown,et al.  Passive electrical constants in three classes of hippocampal neurons. , 1981, Journal of neurophysiology.

[7]  P. Schwartzkroin,et al.  Local circuit synaptic interactions in hippocampal brain slices , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  M. Frotscher,et al.  Neurogenesis of GABAergic neurons in the rat dentate gyrus: A combined autoradiographic and immunocytochemical study , 1985, Neuroscience Letters.

[9]  P. Schwartzkroin,et al.  Characteristics of CA1 neurons recorded intracellularly in the hippocampalin vitro slice preparation , 1975, Brain Research.

[10]  W. Oertel,et al.  Immunocytochemical localization of glutamate decar☐ylase in rat cerebellum with a new antiserum , 1981, Neuroscience.

[11]  P. Schwartzkroin,et al.  Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus , 1985, The Journal of comparative neurology.

[12]  S. Laurberg,et al.  Commissural and intrinsic connections of the rat hippocampus , 1979, The Journal of comparative neurology.

[13]  T. Kosaka,et al.  GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus , 1984, Brain Research.

[14]  D. Prince,et al.  Electrophysiology of dentate gyrus granule cells. , 1984, Journal of neurophysiology.

[15]  M. Frotscher,et al.  Identification of projecting neurons in rat neostriatal slices , 1984, Brain Research.

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

[17]  E. Kandel,et al.  Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. , 1961, Journal of neurophysiology.

[18]  R. Nicoll,et al.  Feed‐forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro , 1982, The Journal of physiology.

[19]  D. Prince,et al.  Anomalous inward rectification in hippocampal neurons. , 1979, Journal of neurophysiology.

[20]  P. Schwartzkroin,et al.  Physiological and morphological identification of a nonpyramidal hippocampal cell type , 1978, Brain Research.

[21]  P. Somogyi,et al.  Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin- or cholecystokinin- immunoreactive material , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  E. Kandel,et al.  ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: III. FIRING LEVEL AND TIME CONSTANT. , 1961, Journal of neurophysiology.

[23]  J. Storm-Mathisen,et al.  First visualization of glutamate and GABA in neurones by immunocytochemistry , 1983, Nature.

[24]  E. Kandel,et al.  Electrophysiology of hippocampal neurons. I. Sequential invasion and synaptic organization. , 1961, Journal of neurophysiology.

[25]  J. Eccles,et al.  PATHWAY OF POSTSYNAPTIC INHIBITION IN THE HIPPOCAMPUS. , 1964, Journal of neurophysiology.

[26]  M. Santini,et al.  Hyperpolarizing increase in membrane conductance in hippocampal neurons. , 1968, Brain research.

[27]  W. Cowan,et al.  Evidence for collateral projections by neurons in Ammon's horn, the dentate gyrus, and the subiculum: a multiple retrograde labeling study in the rat , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[28]  J. Eccles,et al.  LOCATION OF POSTSYNAPTIC INHIBITORY SYNAPSES ON HIPPOCAMPAL PYRAMIDS. , 1964, Journal of neurophysiology.

[29]  L. Sternberger,et al.  THE UNLABELED ANTIBODY ENZYME METHOD OF IMMUNOHISTOCHEMISTRY PREPARATION AND PROPERTIES OF SOLUBLE ANTIGEN-ANTIBODY COMPLEX (HORSERADISH PEROXIDASE-ANTIHORSERADISH PEROXIDASE) AND ITS USE IN IDENTIFICATION OF SPIROCHETES , 1970, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[30]  P. Somogyi,et al.  A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry , 1982, Neuroscience.

[31]  Howard V. Wheal,et al.  In vivo and in vitro studies on putative interneurones in the rat hippocampus: Possible mediators of feed-forward inhibition , 1984, Brain Research.

[32]  R. Chronister,et al.  Organization of projection neurons of the hippocampus , 1979, Experimental Neurology.

[33]  A. Alonso,et al.  Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain , 1982, Neuroscience Letters.

[34]  M. Frotscher,et al.  Commissural afferents innervate glutamate decarboxylase immunoreactive non-pyramidal neurons in the guinea pig hippocampus , 1984, Neuroscience Letters.

[35]  P. Somogyi,et al.  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 , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  T. Berger,et al.  Hippocampal polymorph neurons are the cells of origin for ipsilateral association and commissural afferents to the dentate gyrus , 1981, Brain Research.

[37]  D. Amaral A golgi study of cell types in the hilar region of the hippocampus in the rat , 1978, The Journal of comparative neurology.

[38]  W. Levy,et al.  Anatomical evidence for interlamellar inhibition in the fascia dentata , 1978, Brain Research.