Scientific Understanding of Consciousness
Dendritic Trees properties in Cortical Interneuron subtypes
Scientific Reports 1, 8903 May 2011
Conserved properties of dendritic trees in four cortical interneuron subtypes
Yoshiyuki Kubota, Fuyuki Karube, Masaki Nomura, Allan T. Gulledge, Atsushi Mochizuki, Andreas Schertel & Yasuo Kawaguchi
Division of Cerebral Circuitry, National Institute for Physiological Sciences, Okazaki. 444-8787, Japan
Department of Physiological Sciences, The Graduate University for Advanced Studies (SOKENDAI), Okazaki. 444-8585, Japan
Japan Science and Technology Agency, Core Research for Evolutional Science and Technology, Tokyo, 102-0075, Japan
Laboratory for Cellular Systems Modeling, RIKEN Research Center for Allergy and Immunology (RCAI), Yokohama, 230-0045, Japan
Department of Physiology and Neurobiology, Dartmouth Medical School, Lebanon, NH 03756, U.S.A
Theoretical Biology Laboratory, RIKEN Advanced Science Institute, Wako, 351-0198, Japan
Carl Zeiss NTS GmbH, Carl-Zeiss-Str. 56, D-73447 Oberkochen, Germany
Dendritic trees influence synaptic integration and neuronal excitability, yet appear to develop in rather arbitrary patterns. Using electron microscopy and serial reconstructions, we analyzed the dendritic trees of four morphologically distinct neocortical interneuron subtypes to reveal two underlying organizational principles common to all. First, cross-sectional areas at any given point within a dendrite were proportional to the summed length of all dendritic segments distal to that point. Consistent with this observation, total cross-sectional area was almost perfectly conserved at bifurcation points. Second, dendritic cross-sections became progressively more elliptical at more proximal, larger diameter, dendritic locations. Finally, computer simulations revealed that these conserved morphological features limit distance dependent filtering of somatic EPSPs and facilitate distribution of somatic depolarization into all dendritic compartments. Because these features were shared by all interneurons studied, they may represent common organizational principles underlying the otherwise diverse morphology of dendritic trees.
Our results reveal several features of dendritic structure that underlie the otherwise diverse and variable morphologies of dendritic trees. First, dendritic cross-sectional areas were found to be proportional to the total lengths of all distal dendritic segments, regardless of the number of distal branch points. Second, nonpyramidal neuron dendrites were found to be elliptical, rather than circular, with the degree of ellipticity decreasing with dendritic size and increasing with distance from the soma. This feature tends to limit the variability of surface-area to volume ratios along dendrites. Finally, we found branch points conserve the total cross-sectional area of the parent dendrite. The close match between parent and daughter dendrite cross-sectional area may optimize microtubule-dependent transport within dendrites, and may promote efficient electrical distribution of somatic depolarization into dendritic branches, a process that can reduce the influence of dendritic topology on neuron excitability. This morphological property also optimized the fidelity of EPSP propagation to the soma. In addition, we found that, across all neuron subtypes, somatic volume and surface areas are predictive of total dendritic volumes and surface areas. While our results were obtained from the neurons of adolescent rats, we found similar results in immunohistochemically stained dendrites of nonpyramidal cells in the cortex of adult rats fixed in vivo.
The linear relationship between the cross-sectional area and the total dendritic length of all dendrites distal to that point indicates that dendrites taper smoothly, independent of branch points, a morphological feature that may facilitate efficient intracellular transport into dendritic trees by allowing an initially large number of microtubules near the base of the dendrite to course continuously from the soma to all distal dendritic endpoints. The conservation of total cross-sectional area at branch points is consistent with this hypothesis in allowing even distribution of trafficked molecules into the dendritic tree. Indeed, in two interneuron branch points examined for microtubule content, we found that the total number of microtubules in daughter branches was almost identical to the number found in the parent dendrite.
The irregular elliptic shape of dendritic cross-sections may provide more efficient packing of neuropil within small volumes of space, especially given the presence of fibers coursing in all directions (vertically, horizontally, and radially) through the tissue. Additional studies of neuron packing efficiency are needed to determine if elliptic dendritic segments are indeed advantageous for neuropil organization. Alternatively, elliptical cross-sections at proximal locations will tend to preserve surface area to volume ratios along dendrites. Indeed, we found that dendrites have a fairly constant surface area to volume ratio at locations more distal than 30–40 µm from soma. This may benefit neurons by normalizing gas exchange and molecular diffusion into compartments having different diameters. It would also tend to normalize cytosolic ion concentrations following activation of ion channels uniformly distributed in the dendritic membrane. For instance, it could allow given density of calcium channels to produce a standardized intracellular calcium concentration, independent of dendritic location, to preserve the fidelity of Ca-protein interactions.
Changes in dendritic morphology are well documented in neurodegenerative diseases. Our data suggest that, in healthy neurons, dendritic structure is more precisely regulated than might be guessed given the diversity of dendritic tree morphologies. It will be important for future work to assess the detailed morphology of dendrites in pathological tissue to test if alterations in dendritic tapering and branch point uniformity might participate in generating the cognitive deficits associated with disease.
Together, our data from four different nonpyramidal cell subtypes reveal morphological features of dendritic trees that appear well suited to allow the uniform retrograde distribution of molecules and electrical signals into dendritic trees, while at the same time, enhancing the anterograde synaptic signal conduction and limiting the effect of dendritic topology on action potential output. Because these features are conserved across cortical nonpyramidal cell subtypes that differ greatly in sizes, shape, and functions within cortical circuits, it is likely that these features of dendrites are common to the dendrites of many neuron types throughout the brain.
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