GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus

The hippocampus, in particular the neocortex–hippocampus–neocortex circuit, is widely believed to be crucial in memory. Information flow in this circuit is strongly influenced by relatively sparse afferents derived from subcortical centres, such as the septum, involved in arousal, emotions and autonomic control. A powerful mechanism, by which numerically small inputs can produce profound effects, is feed-forward inhibition1, that is, the activation of local inhibitory interneurons, which, in turn, control the activity of large populations of principal cells in the hippocampus. An example is the cholinergic input to the hippocampus from the septum, which is likely to be involved in feed-forward operations2–8. Here, we demonstrate the existence of a circuit underlying another powerful mechanism of subcortical control of hippocampal information processing. We show that GABA-containing afferents originating in the septum innervate most of the GABA-containing interneurons in the hippocampus, making many synaptic contacts with each of them. Activation of the GABA-containing neurons in the septum is likely to lead to disinhi-bition of the principal neurons in the hippocampal formation and so this pathway is probably crucial in the induction of hippocampal electrical activity patterns, and may be involved in NMDA (N-methyl-D-aspartate) receptor-mediated functions, such as memory9, in a permissive manner.

[1]  H. Petsche,et al.  [The significance of the rabbit's septum as a relay station between the midbrain and the hippocampus. I. The control of hippocampus arousal activity by the septum cells]. , 1962, Electroencephalography and clinical neurophysiology.

[2]  K. Toyama,et al.  Long-term potentiation investigated in a slice preparation of striate cortex of young kittens , 1981, Neuroscience Letters.

[3]  Y. Ben-Ari,et al.  Intracellular observations on the disinhibitory action of acetylcholine in the hippocampus , 1981, Neuroscience.

[4]  R. Dingledine,et al.  The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro , 1981, Brain Research.

[5]  G. V. Goddard,et al.  Septal modulation of the population spike in the fascia dentata produced by perforant path stimulation in the rat , 1982, Brain Research.

[6]  J. Miller,et al.  Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat , 1982, Brain Research.

[7]  D. Prince,et al.  Cholinergic excitation of mammalian hippocampal pyramidal cells , 1982, Brain Research.

[8]  J. Miller,et al.  Calcium-binding protein distribution in the rat brain , 1982, Brain Research.

[9]  G. Collingridge,et al.  Excitatory amino acids in synaptic transmission in the Schaffer collateral‐commissural pathway of the rat hippocampus. , 1983, The Journal of physiology.

[10]  G. Buzsáki,et al.  Cellular bases of hippocampal EEG in the behaving rat , 1983, Brain Research Reviews.

[11]  H. Wigström,et al.  Facilitated induction of hippocampal long-lasting potentiation during blockade of inhibition , 1983, Nature.

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

[13]  M. Mesulam,et al.  Cholinergic and non-cholinergic septohippocampal pathways , 1985, Neuroscience Letters.

[14]  P. Somogyi,et al.  The Journal of Histochemistry and Cytochemistry Copyright Iii. Demonstration of Gaba in Golgi-impregnated Neurons and in Conventional Electron Microscopic Sections of Cat Striate Cortex' , 2022 .

[15]  P. Somogyi,et al.  Antisera to gamma-aminobutyric acid. I. Production and characterization using a new model system. , 1985, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[16]  Michael Frotscher,et al.  Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study , 1985, The Journal of comparative neurology.

[17]  G. V. Goddard,et al.  Medial septal facilitation of hippocampal granule cell activity is mediated by inhibition of inhibitory interneurones , 1985, Brain Research.

[18]  G. Collingridge,et al.  A selective N-methyl-d-aspartate antagonist depresses epileptiform activity in rat hippocampal slices , 1985, Neuroscience Letters.

[19]  G. Lynch,et al.  Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation , 1986, Brain Research.

[20]  M. Celio,et al.  Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. , 1986, Science.

[21]  R. Dingledine,et al.  Involvement of N-methyl-d-aspartate Receptors in Involvement of N-methyl-d-aspartate Receptors in Epileptiform Bursting in the Rat Hippocampal Slice , 2008 .

[22]  G. Lynch,et al.  Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 , 1986, Nature.

[23]  H. Katsumaru,et al.  GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus , 1987, Brain Research.

[24]  C. Nyakas,et al.  Detailed projection patterns of septal and diagonal band efferents to the hippocampus in the rat with emphasis on innervation of CA1 and dentate gyrus , 1987, Brain Research Bulletin.

[25]  W. Singer,et al.  Long-term potentiation and NMDA receptors in rat visual cortex , 1987, Nature.

[26]  C. Pavlides,et al.  Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm , 1988, Brain Research.

[27]  R. Lester,et al.  Synaptic activation of N‐methyl‐D‐aspartate receptors in the Schaffer collateral‐commissural pathway of rat hippocampus. , 1988, The Journal of physiology.