Abstract
In slices of guinea-pig brains, 36 neurons located in the mediolateral part of the lateral septum were stained intracellularly with horseradish peroxidase (n=28) or biocytin (n=8) after electrophysiological characterization. These neurons belonged to class A neurons (n=23), which generated pronounced Ca++-dependent high-threshold spikes in control medium, or to class C neurons (n=9), which were recognized by the occurrence of small-amplitude sodic spikes followed by slower larger calcic spikes. The present results demonstrate that, despite the variety of individual cell types, the major morphological population (30/36 cells) was composed of a homogeneous class of large-sized neurons that displayed thick primary dendrites and abundant dendritic appendages. The remaining 6 cells were small-sized, poorly-spiny neurons. Somatic spines were observed on 5 out of the 30 large cells and on one out of the six smaller cells. Labeled axons were mainly oriented to the anterior commissure. The axons of nine cells richly collateralized near the perikaryon. Ultrastructural examination of 3 horseradish peroxidase-injected cells showed indented nuclei, classic organelles and somatic spines. Terminal boutons established symmetric synapses with the injected cells. These results describe the morphological features of electrophysiologically identified neurons and indicate that class A and class C neurons are distributed among morphological populations differing in perikaryal size. This suggests that the different electrical properties of class A and class C neurons reflect recordings from different parts of the neuron rather than from neurons of different types. Furthermore, the present findings demonstrate that, in the guinea-pig, electrical and morphological characteristics of somatospiny neurons are comparable with those of non-somatospiny neurons. Somatospiny neurons have a recognized integrative role in the hippocampo-septo-hypothalamic complex.
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References
Alonso JR, Frotscher M (1989) Organization of the septal region in the rat brain. A Golgi/EM study of lateral septal neurons. J Comp Neurol 286:472–487
Beauvillain JC, Poulain P, Tramu G (1983) Immunocytochemical localization of enkephalin in the lateral septum of the guinea-pig brain. Cell Tissue Res 228:265–276
Beauvillain JC, Mitchell V, Tramu G, Mazzuca M (1991) GABA and enkephalin in the lateral septum of the guinea-pig: light and electron microscopic evidence for interrelations J Comp Neurol 308:103–114
Carette B, Poulain P, Doutrelant O (1992) Electrical properties of neurons in the mediolateral part of the lateral septum: intracellular recordings from guinea-pig brain slices. Exp Brain Res 91:105–114
De France JF (1976) A functional analysis of the septal nuclei. In: De France JF (ed) The septal nuclei. Advances in behavioral biology, vol 20. Plenum Press. New York London, pp 185–227
Doutrelant O, Martin-Bouyer L, Poulain P (1992) Morphological analysis of the neurons in the area of the hypothalamic magnocellular dorsal nucleus of the guinea-pig. Cell Tissue Res 269:107–117
Gall C, Moore RY (1984) Distribution of enkephalin, substance P, tyrosine hydroxylase and 5-hydroxytryptamine immunoreactivity in the septal region of the rat. J Comp Neurol 225:212–227
Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25:1–11
Jakab RL, Leranth C (1990a) Somatospiny neurons in the rat lateral septal area are synaptic targets of hippocamposeptal fibers: a combined EM/Golgi and degeneration study. Synapse 6:10–22
Jakab RL, Leranth C (1990b) Catecholaminergic, GABAergic, and hippocamposeptal innervation of GABAergic “somatospiny” neurons in the rat lateral septal area. J Comp Neurol 302:305–321
Jakab RL, Leranth C (1991) Synaptology and origin of somatostatin fibers in the rat lateral septal area: convergent somatostatinergic and hippocampal inputs of somatospiny neurons. Brain Res 565:123–134
Jakab RL, Naftolin F, Leranth C (1991) Convergent vasopressinergic and hippocampal input onto somatospiny neurons of the rat lateral septal area. Neuroscience 40:413–421
Kita H, Armstrong W (1991) A biotin-containing compound N-(2-aminoethyl) biotinamide for intracellular labeling and neuronal tracing studies: comparison with biocytin. J Neurosci Methods 37:141–150
Köhler C, Chan-Palay V, Steinbusch H (1982) The distribution and origin of serotonin-containing fibers in the septal area: a combined immunohistochemical and fluorescent retrograde tracing study in the rat. J Comp Neurol 209:91–111
Leranth C, Deller T, Buzsaki G (1992) Intraseptal connections redefined: lack of a lateral septum to medial septum path. Brain Res 583:1–11
Meibach RC, Siegel A (1977) Efferent connections of the hippocampal formation in the rat. Brain Res 124:197–224
Metz CB, Schneider SP, Fyffe REW (1989) Selective suppression of endogenous peroxidase activity: application for enhancing appearance of HRP-labeled neurons in vitro. J Neurosci Methods 26:181–188
Nauta WJH (1958) Hippocampal projections and related neural pathways to the midbrain in the cat. Brain Res 81:319–340
Onteniente B, Menetrey D, Arai R, Calas A (1989) Origin of the met-enkephalinergic innervation of the lateral septum in the rat. Cell Tissue Res 256:585–592
Osen KK (1969) Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136:453–484
Phelan DK, Hasuo H, Twery MJ, Gallagher JP (1989) Projection neurons in the rat dorsolateral septal nucleus possess recurrent axon collaterals. Jeurosci Lett 97:259–265
Poulain P (1974) L'hypothalamus et le septum du cobaye de 400 grammes en coordonnées stéréotaxiques. Arch Anat Micros Morphol Exp 63:37–50
Poulain P, Martin-Bouyer L, Beauvillain JC, Tramu G (1984) Study of the efferent connections of the enkephalinergic magnocellular dorsal nucleus in the guinea-pig hypothalamus using lesions, retrograde tracing and immunocytochemistry: evidence for a projection to the lateral septum. Neuroscience 11:331–343
Raisman G (1966) The connections of the septum. Brain 89:317–348
Sakanaka M, Magari S (1989) Reassessment of enkephalin (ENK)-containing afferents to the rat lateral septum with reference to the fine structures of septal ENK fibers. Brain Res 479:205–216
Sar M, Stumpf WE, Miller RJ, Chang KJ, Cuatrecasas P (1978) Immunohistochemical localization of enkephalin in rat brain and spinal cord. J Comp Neurol 182:17–38
Staiger JF, Nürnberger F (1991a) The efferent connections of the lateral septal nucleus in the guinea-pig: intrinsic connectivity of the septum and projections to other telencephalic areas. Cell Tissue Res 264:415–426
Staiger JF, Nürnberger F (1991b) The efferent connections of the lateral septal nucleus in the guinea-pig: projections to the diencephalon and brainstem. Cell Tissue Res 264:391–413
Staiger JF, Wouterlood FG (1990) Efferent projections from the lateral septal nucleus to the anterior hypothalamus in the rat: a study combining Phaseolus vulgaris-leucoagglutinin tracing with vasopressin immunocytochemistry. Cell Tissue Res 261:17–23
Stengaard-Pedersen K, Larsson LI (1981) Comparative immunocytochemical localization of putative opioids ligands in the central nervous system. Histochemistry 73:89–114
Swanson LW, Cowan WM (1977) An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172:49–84
Swanson LW, Cowan WM (1979) The connections of the septal region in the rat. J Comp Neurol 186:621–656
Tokuno H, Nakamura Y, Kudo M, Kitao Y (1990) Effect of Triton X-100 in the Golgi-Kopsch method. J Neurosci Methods 35:75–77
Tramu G, Beauvillain JC, Croix D, Leonardelli J (1981) Comparative localization of enkephalin and somatostatin in the median eminence, hypothalamus and adjacent areas in the guinea-pig brain. Brain Res 215:235–255
Tseng GF, Parada I, Prince DA (1991) Double-labeling with rhodamine beads and biocytin: a technique for studying corticospinal and other projection neurons in vitro. J Neurosci Methods 37:121–131
Twery MJ, Phelan KD, Gallagher JP (1992) Spontaneous bursting and non-bursting activity in morphologically identified neurons of the rat dorsolateral septal nucleus in vitro. Neuroscience 46:669–679
Witter MP, Daelmans HEM, Jorritsma-Byham B, Staiger JF, Wouterlood FG (1992) Restricted origin and distribution of projections from the lateral to the medial septal complex in rat and guinea-pig. Neurosci Lett 148:164–168
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Doutrelant, O., Poulain, P., Carette, B. et al. Light- and electron-microscopic study of electrophysiologically characterized neurons in the mediolateral part of the lateral septum of the guinea-pig. Cell Tissue Res 275, 543–553 (1994). https://doi.org/10.1007/BF00318823
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DOI: https://doi.org/10.1007/BF00318823