Elsevier

Neuroscience

Volume 172, 13 January 2011, Pages 74-93
Neuroscience

Cellular and Molecular Neuroscience
Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices

https://doi.org/10.1016/j.neuroscience.2010.10.047Get rights and content

Abstract

Based on the specificity of its inputs and targets, the lateral habenular complex (LHb) constitutes a pivotal motor-limbic interface implicated in various cerebral functions particularly in regulating monoamine transmission. Despite its functional significance, cellular characteristics underlying LHb functionality have not been examined systematically. The present study aimed to correlate morphological and electrophysiological properties of neurons within the different subnuclei of the LHb using whole-cell recording and neurobiotin labeling in rat slice preparations. Morphological analysis revealed a heterogeneous population of projection neurons randomly distributed throughout the LHb. According to somatodendritic characteristics four main categories were classified including spherical, fusiform, polymorphic and vertical cells. Electrophysiological characterization of neurons within the different categories demonstrated homologous profiles and no significant differences between groups. Typically, LHb neurons possessed high input resistances and long membrane time constants. They also displayed time-dependent inward rectification and distinct afterhyperpolarization. A salient electrophysiological feature of LHb neurons was their ability to generate rebound bursts of action potentials in response to membrane hyperpolarization. Based on the pattern of spontaneous activity, neurons were classified as silent, tonic or bursting. The occurrence of distinctive firing modes was not related to topographic allocation. The patterns of spontaneous firing and evoked discharge were highly sensitive to alterations in membrane potential and merged upon de- and hyperpolarizing current injection and synaptic stimulation. Besides projection neurons, recordings revealed the existence of a subpopulation of cells possessing morphological and physiological properties of neocortical neurogliaform cells. They were considered to be interneurons. Our data suggest that neurons within the different LHb subnuclei behave electrophysiologically more similar than expected, considering their morphological heterogeneity. We conclude that the formation of functional neuronal entities within the LHb may be achieved through defined synaptic inputs to particular neurons, rather than by individual neuronal morphologies and intrinsic membrane properties.

Research Highlights

▶ The rat LHb comprises a morphological heterogeneous population of projection neurons. ▶ Defined cell morphologies are not related to distinct electrophysiological phenotypes. ▶Distinct LHb neuron functionalities depend on particular afferent connectivity.

Section snippets

Slice preparation

Brain slices were prepared from 10 to 21-d old Wistar rats, which were obtained from an institutional breeder (Forschungseinrichtungen für Experimentelle Medizin, Charité-Universitätsmedizin Berlin, Krahmerstraβe 6–10, D-12207 Berlin, Germany). All experiments were approved by the Regional Berlin Animals Ethics Committee (T0127/02) and performed in strict accordance with the European Communities Council directive regarding care and use of animals for experimental procedures. All efforts were

Results

The data presented in this study are based on intracellular recordings obtained from 102 neurons in habenular slice preparations of 53 rats. Eighty-five neurons were adequately labeled with neurobiotin and recovered morphologically. Of these, 74 neurons were located within the LHb. Another 11 neurons were situated in the medial habenular complex.

Discussion

In the present study, we describe for the first time a detailed investigation of morphological and electrophysiological properties of identified LHb neurons in relation to subnucleus specificity of their distribution within the lateral habenular complex. Our main observation is that distinct morphologies of projection neurons within the different subnuclei are not related to certain membrane properties and/or modes of electrical responsiveness. Despite differences in cytoarchitecture, LHb

Conclusion

This investigation was based on the assumption that correlations between morphological characteristics, intrinsic membrane properties and spontaneous firing patterns of individual LHb neurons could help defining the identity and relevance of the different LHb subnuclei recently discovered in the lateral habenula of rats. Having recorded from neurons in almost all subnuclei, we conclude that LHb neurons form an electrophysiologically more homogenous cell population than anticipated, given the

Acknowledgments

We thank H. Meyer and R. Lommel for excellent technical assistance, J. Roeper for generous technical and conceptual support, and R. Bernard for helpful discussions and critically review of the manuscript.

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