It is often assumed that highly-branched neuronal structures perform compartmentalized computations. However, previously we showed that the Gastric Mill (GM) neuron in the crustacean stomatogastric ganglion (STG) operates like a single electrotonic compartment, despite having thousands of branch points and total cable length >10 mm (Otopalik et al., 2017a; 2017b). Here we show that compact electrotonic architecture is generalizable to other STG neuron types, and that these neurons present direction-insensitive, linear voltage integration, suggesting they pool synaptic inputs across their neuronal structures. We also show, using simulations of 720 cable models spanning a broad range of geometries and passive properties, that compact electrotonus, linear integration, and directional insensitivity in STG neurons arise from their neurite geometries (diameters tapering from 10-20 µm to < 2 µm at their terminal tips). A broad parameter search reveals multiple morphological and biophysical solutions for achieving different degrees of passive electrotonic decrement and computational strategies in the absence of active properties.
Microscale connectomics involves the large-scale acquisition of high resolution serial electron micrographs from which neuronal arbors can be reconstructed and synapses detected. In addition to connectivity information, these datasets are also rich with structural information including vesicle types, number of postsynaptic partners at a given presynaptic site, and spatial distribution of synaptic inputs and outputs. Using serial blockface scanning electron microscopy (SBEM), we collected two volumes of serial EM data from ganglia of the medicinal leech. In the first volume, we sampled a small fraction of the neuropil belonging to an adult ganglion. From this dataset we measured the proportion of arbors that contain vesicles, the types of vesicles contained, and developed criteria to identify synapses and measure the number of apparent postsynaptic partners in apposition to presynaptic boutons. In the second dataset, we sampled an entire juvenile ganglion, which included the somata and arbors of all the neurons. We used this dataset to put our findings from mature tissue into the context of fully reconstructed arbors and to explore the spatial distribution of synaptic inputs and outputs on these arbors. We observed that some neurons segregate their arbors into input-only and mixed input/output zones, that other neurons contained exclusively mixed input/output zones, and that still others contained only input zones. These results provide a groundwork for future behavioral studies.
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