Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus

Journal of Neuroscience

Volumn 19, Issue 22, 1999, Pages 10082-10097

  Gulyás, Attila I ^a   Megías, Manuel ^a   Emri, Zsuzsa ^a   Freund, Tamás F ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

3D; Database for modeling; Dendrite geometry; Electron microscopy; GABA; Inhibitory neurons; Serial reconstruction; Synaptic convergence

Indexed keywords

4 AMINOBUTYRIC ACID; CALBINDIN; CALRETININ; PARVALBUMIN;

ANIMAL TISSUE; ARTICLE; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; GABAERGIC SYSTEM; HIPPOCAMPUS; INTERNEURON; MALE; NERVE CELL NETWORK; NEUROANATOMY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; RAT; SYNAPSE; TISSUE DISTRIBUTION;

EID: 0343362706     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-22-10082.1999     Document Type: Article

References (42)

1. Acsady L, Gorcs TJ, Freund TF (1996) Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 73:317-334.
2. Ali AB, Thomson AM (1998) Facilitating pyramid to horizontal oriens-alveus interneurone inputs: dual intracellular recordings in slices of rat hippocampus. J Physiol (Lond) 507: 185-199.
3. Amaral DG, Witter MP (1989) The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31:571-591.
4. Baimbridge KG, Miller JJ (1982) Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat. Brain Res 245:223-229.
5. Banks MI, Li TB, Pearce RA (1998) The synaptic basis of GABAA,slow. J Neurosci 18:1305-1317.
6. Blasco-Ibanez JM, Freund TF (1995) Synaptic input of horizontal interneurons in stratum oriens of the hippocampal CA1 subfield: structural basis of feed-back activation. Eur J Neurosci 7:2170-2180.
7. Buhl EH, Halasy K, Somogyi P (1994) Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites. Nature 368:823-828.
8. Buzsaki G, Chrobak JJ (1995) Temporal structure in spatially organized neuronal ensembles: a role for interneuronal networks. Curr Opin Neurobiol 5:504-510.
9. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378:75-78.
10. Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336: 170-173.
11. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:345-470.
12. Freund TF, Gulyás AI, Acsady L, Gorcs T, Toth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci USA 87:8501-8505.
13. 28k-immunoreactive interneurons in the hip-pocampus. Hippocampus 6:525-534.
14. Gulyás AI, Miettinen R, Jacobowitz DM, Freund TF (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus-I. A new type of neuron specifically associated with the mossy fibre system. Neuroscience 48:1-27.
15. Gulyás AI, Miles R, Hájos N, Freund TF (1993a) Precision and variability in postsynaptic target selection of inhibitory cells in the hippocampal CA3 region. Eur J Neurosci 5:1729-1751.
16. Gulyás AI, Miles R, Sik A, Toth K, Tamamaki N, Freund TF (1993b) Hippocampal pyramidal cells excite inhibitory neurons through a single release site. Nature 366:683-687.
17. Gulyás AI, Hájos N, Freund TF (1996) Interneurons containing calretinin are specialized to control other interneurons in the rat hippocampus. J Neurosci 16:3397-3411.
18. Halasy K, Buhl EH, Lorinczi Z, Tamas G, Somogyi P (1996) Synaptic target selectivity and input of GABAergic basket and bistratified interneurons in the CA1 area of the rat hippocampus. Hippocampus 6:306-329.
19. Hodgson AJ, Penke B, Erdei A, Chubb IV, Somogyi P (1985) Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J Histochem Cytochem 33:229-239.
20. 2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119-130.
21. Li XG, Somogyi JM, Tepper JM, Buzsaki G (1992) Axonal and dendritic arborization of an intracellularly labelled chandelier cell in the CA1 region of rat hippocampus. Exp Brain Res 90:519-525.
22. McBain CJ, DiChiara TJ, Kauer JA (1994) Activation of metabotropic glutamate receptors differentially affect two classes of hippocampal interneurons and potentiates excitatory synaptic transmission. J Neurosci 14:4433-4445.
23. Miettinen R, Freund TF (1992) Convergence and segregation of septal and median raphe inputs onto different subsets of hippocampal inhibitory interneurons. Brain Res 594:263-272.
24. Miettinen R, Gulyás Al, Baimbridge KG, Jacobowitz DM, Freund TF (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus-II. Co-existence with other calcium binding proteins and GABA. Neuroscience 48:29-43.
25. Miles R, Toth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
26. Mulloney B, Perkel DH, Budelli RW (1981) Motor-pattern production: interaction of chemical and electrical synapses. Brain Res 229:25-33.
27. Oleskevich S, Descarries L, Watkins KC, Seguela P, Daszuta A (1991) Ultrastructural features of the serotonin innervation in adult rat hippocampus: an immunocytochemical description in single and serial thin sections. Neuroscience 42:777-791.
28. Pearce RA (1993) Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10:189-200.
29. Perkel DH, Mulloney B (1974) Motor pattern production in reciprocally inhibitory neurons exhibiting postinhibitory rebound. Science 185:181-183.
30. Pierce JP, Lewin GR (1994) An ultrastructural size principle. Neuroscience 58:441-446.
31. Rogers JH (1989) Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31:697-709.
32. Sik A, Tamamaki N, Freund TF (1993) Complete axon arborization of a single CA3 pyramidal cell in the rat hippocampus, and its relationship with postsynaptic parvalbumin-containing interneurons. Eur J Neurosci 5:1719-1728.
33. 28k) 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.
34. Soltesz I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283.
35. Somogyi P, Hodgson AJ (1985) Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J Histochem Cytochem 33:249-257.
36. 28k-containing nonpyramidal cells in the rat hippocampus: their immunoreactivity for GABA and projection to the medial septum. Neuroscience 49:793-805.
37. Traub RD, Whittington MA, Colling SB, Buzsaki G, Jefferys JG (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol (Lond) 493:471-484.
38. Umbriaco D, Garcia S, Beaulieu C, Descarries L (1995) Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5:605-620.
39. Wang X-J, Rinzel J (1993) Spindle rhythmicity in the reticularis thalami nucleus: Synchronization among mutually inhibitory neurons. Neuroscience 53:899-904.
40. Whittington MA, Traub RD, Jeffreys JG (1995) Synchronized oscillations in interneurons driven by metabotropic glutamate receptor activation. Nature 373:612-615.
41. Wolf E, Birinyi A, Pomahazi S (1995) A fast 3-dimensional neuronal tree reconstruction system that uses cubic polynomials to estimate dendritic curvature. J Neurosci Methods 63:137-145.
42. Wouterlood FG, Saldana E, Witter MP (1990) Projection from the nucleus reuniens thalami to the hippocampal region: light and electron microscopic tracing study in the rat with the anterograde tracer Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 296:179-203.