Developmental Changes in Dendritic Shape and Synapse Location Tune Single-Neuron Computations to Changing Behavioral Functions

Abstract

During nervous system development, different classes of neurons obtain different dendritic architectures, each of which receives a large number of input synapses. However, it is not clear whether synaptic inputs are targeted to specific regions within a dendritic tree and whether dendritic tree geometry and subdendritic synapse distributions might be optimized to support proper neuronal input-output computations. This study uses an insect model where structure and function of an individually identifiable neuron, motoneuron 5 (MN5), are changed while it develops from a slow larval crawling into a fast adult flight motoneuron during metamorphosis. This allows for relating postembryonic dendritic remodeling of an individual motoneuron to developmental changes in behavioral function. Dendritic architecture of MN5 is analyzed by three-dimensional geometric reconstructions and quantitative co-localization analysis to address the distribution of synaptic terminals. Postembryonic development of MN5 comprises distinct changes in dendritic shape and in the subdendritic distribution of GABAergic input synapses onto MN5. Subdendritic synapse targeting is not a consequence of neuropil structure but must rely on specific subdendritic recognition mechanisms. Passive multicompartment simulations indicate that postembryonic changes in dendritic architecture and in subdendritic input synapse distributions may tune the passive computational properties of MN5 toward stage-specific behavioral requirements.

ShakerandShalMediate Transient Calcium-Independent Potassium Current in a Drosophila Flight Motoneuron

“…1A). As is the case with most insect motoneurons, the soma does not generate action potentials but is mostly passive (Duch and Levine 2000;Duch et al 2008;Meseke et al 2009). The dendrites of MN5 span large parts of the dorsal mesothoracic motor neuropil (Fig.…”

“…The import of the reconstructed geometries of MN5 into NEURON was done as described earlier (Evers et al 2005). As values for the passive electrical properties of MN5, we used values commonly applied for vertebrate and invertebrate neurons (Meseke et al 2009) (specific membrane capacity, C m ϭ 1.15*10 Ϫ6 F*cm Ϫ2 , axoplasmic resistance R a ϭ 90 ⍀*cm, passive leak conductance g_pas ϭ 0.0001667 ⍀ Ϫ1 cm Ϫ2 ). These values were consistent with measured values of whole cell input resistance and whole cell capacitance as recorded from the soma of MN5.…”

“…7C, see arrows). We have previously published methods for co-localization analyses of immunolabeled structures and reconstructed dendritic surfaces (Duch and Mentel 2004;Evers et al 2005;Meseke et al 2009;Schmitt et al 2004). In the representative example in Fig.…”

Tiling among stereotyped dendritic branches in an identified Drosophila motoneuron

“…1A). As is the case with most insect motoneurons, the soma does not generate action potentials but is mostly passive Duch et al, 2008;Meseke et al, 2009). The dendrites of MN5 span large parts of the dorsal mesothoracic motor neuropil and sprout off a primary neurite connecting the cell body with the axon (Fig.…”

“…We conducted branch order analysis by defining the primary neurite as origin, with the branch order 0, as described in previous studies (see Materials and Methods;Evers et al, 2005;Duch et al, 2008;Meseke et al, 2009). This procedure of collapsing the reconstruction onto one virtual origin ensured that all dendrites branching off the primary neurite were considered first-order branches, and the distances and orders of all daughter branches are measured with regard to their branching order relative to this first-order branch.…”