Catecholaminergic, GABAergic, and hippocamposeptal innervation of gabaergic “somatospiny” neurons in the rat lateral septal area

Abstract

This study deals with the neurochemical characterization of the rat lateral septal area (LSA) somatospiny neurons and their innervation by hippocamposeptal, catecholaminergic, and GABAergic fibers. Electron microscopic single and double immunostaining methods were used to label catecholaminergic fibers and GABAergic cells and boutons. Axon terminals originating in the hippocampus were labeled by acute anterograde axon degeneration induced by fimbria-fornix transection 36 hours before sacrifice. Three types of experiments were performed. The convergent catecholaminergic and hippocamposeptal innervation of LSA somatospiny neurons was studied by combining immunostaining for tyrosine hydroxylase (TH) with fimbria-fornix transection. GABAergic neurons and their hippocamposeptal afferents were identified and characterized in colchicine pretreated animals immunostained for glutamic acid decarboxylase (GAD) combined with fimbria-fornix transection. The third experiment aimed at simultaneously visualizing the relationships between catecholaminergic boutons, hippocamposeptal excitatory amino acid containing axon terminals and GABAergic profiles by double immunostaining for TH (the PAP technique) and GAD (the immunogold method) combined with fimbria-fornix transection. The results are summarized as follows: 1) The same LSA somatospiny neurons receive synaptic inputs from the hippocampus and TH immunoreactive fibers which form pericellular baskets around these cells. 2) LSA somatospiny neurons are GABAergic and are postsynaptic targets of GABAergic boutons with unknown origin and hippocamposeptal axon terminals. 3) The double immunostaining experiment, finally, provided direct evidence that the same GABAergic somatospiny neurons are postsynaptic targets of both catecholaminergic and hippocamposeptal afferents. The synaptic interconnections described in this study provide anatomical basis for a better understanding of the action of catecholamines, excitatory amino acids, and GABA on the activity of LSA neurons.

Catecholaminergic innervation of the septum in the frog: A combined immunohistochemical and tract‐tracing study

“…DA is involved in the modulation of the activity at all levels within the septal circuitry: in the regulation of the hippocamposeptal pathway by the influence of glutamatergic hippocampal neurons, in the septohippocampal route over cholinergic cells in the medial septum/diagonal band nucleus (Robinson et al, 1979;Costa et al, 1983), and finally, influencing GABAergic neurons of the lateral septum (Jakab and Leranth, 1990). Robinson and coworkers (1979) demonstrated a role of the mesolimbic DA system in the regulation of the turnover rate of acetylcholine in the hippocampus.…”

“…In addition, DA has a concentrationdependent modulatory effect on other neurotransmitters, such as Glu and ␥-aminobutyric acid (GABA) (Chiodo and Berger, 1986). Jakab and Leranth (1990) suggested that high levels of DA release in the septum can result in depression in the activity of lateral septal neurons, whereas basal levels of DA release can maintain their sensitivity to both excitatory and inhibitory inputs.…”

“…Thus, DA neurons exert a tonic inhibitory effect on acetylcholine metabolism of the septohippocampal pathway. In the lateral septal area, GABAergic spiny neurons receive inputs from CA afferents (Jakab and Leranth, 1990), which provides a morphological basis of the interaction of glutamate and DA.…”

Vesicular glutamate transporter 3-immunoreactive pericellular baskets ensheath a distinct population of neurons in the lateral septum

“…Finally, there is an extensive intrinsic arborization of the axons of GABAergic projection neurons inside the LS organized in subregional circuits (Jakab and Leranth, 1995). These fibers and potential extrinsic, GABAergic sources (Jakab and Leranth, 1990) probably cause the heavy homogeneous VGAT-ir of the LS which was -similar to VGLUT1 and VGLUT2 -only rarely co-expressed with VGLUT3-ir.…”

Differential patterns of c-fos mRNA expression in amygdala during successive stages of odor discrimination learning.

“…Possibly relevant to this, neuroanatomical studies have shown that the ventral lateral septum generates a strong projection to the rostral bed nucleus (Staiger and Nurnberger 1991) including zones targeted by the medial amygdala (Canteras et al 1995), whereas physiological work points to a close relationship between the ventral lateral septum and the bed nucleus (Mathieson et al 1989). The lateral septum, including its ventral aspect, contains high concentrations of GABAergic neurons (Kohler and Chan-Palay 1983;Panula et al 1984;Jakab and Leranth 1990;and others), which would be expected to suppress responses by bed nucleus neurons to activity in the presumably glutamatergic medial amygdala (McDonald and Augustine 1993;Shindou et al 1993;Pitkanen and Amaral 1994). According to this hypothesis, the weaker medial projection to the septum can serve, on some occasions, to cancel the effects of the stronger medial amygdalar projection to the bed nucleus (Canteras et al 1995; see schematic in Fig.…”