Functionally relevant measures of spatial complexity in neuronal dendritic arbors.
We introduce a set of scaling exponents for characterizing global 3D morphologic properties of mass distribution, branching and taper in neuronal dendritic arbors, capable of distinguishing functionally relevant changes in dendritic complexity that standard Sholl analysis and fractal analysis cannot. We demonstrate that the scaling exponent for mass distribution, d(M), comprises a sum of independent scaling exponents for branching, d(N), and taper, d(T). The accuracy of experimental measurements of the scaling exponents was verified using computer generated self-similar binary trees of known fractal dimension, and with prescribed amounts of branching and taper. The theory was applied to measuring 3D spatial complexity in the apical and basal dendritic trees of two functionally distinct types of macaque monkey neocortical pyramidal neurons: long corticocortical projection neurons from superior temporal cortex to area 46 of the prefrontal cortex (PFC), and local projection neurons within area 46 of the PFC. Two distinct scaling subregions (proximal and medial) were identified in both apical and basal trees of the two neuron types, and scaling exponents were fitted. A small but significant difference in mass scaling in the proximal region distinguished long from local projection neurons. Interestingly, both classes of neuron exhibited a homeostatic pattern of mass distribution across the two regions: despite large differences between proximal and medial regions in branching and tapering exponents, these effects were compensatory, resulting in a uniform, slow reduction of mass with distance from the soma, over both scaling regions of the apical and basal trees. Given a uniformly excitable membrane, the electrotonic properties of dendritic arbors depend entirely upon mass distribution, and its relative contributions from dendritic branching and taper. By capturing each of these complex morphologic properties in a single, globally descriptive parameter, the new 3D scaling exponents introduced in this study permit efficient morphometric characterization of complex dendritic arbors in the fewest possible parameters, that can be directly related to their electrotonic properties, and hence to neuronal function.
Rothnie
P
P
Center for Biomathematics, Mount Sinai School of Medicine, New York, 10029-6574, USA.
Kabaso
D
D
Hof
P R
PR
Henry
B I
BI
Wearne
S L
SL
D000818:Animals; D003712:Dendrites / Q000502:physiology / Q000648:ultrastructure*; D006801:Humans; D008252:Macaca fascicularis; D008959:Models, Neurological; D009434:Neural Pathways / Q000502:physiology; D009474:Neurons / Q000502:physiology / Q000648:ultrastructure*; D017966:Pyramidal Cells / Q000502:physiology