Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig

Intracellular recordings from neurons in the dorsal motor nucleus of the vagus (vagal motoneurons, VMs) obtained in the guinea pig brain stem slice preparation were used for both horseradish peroxidase (HRP) labeling of the neurons and for measurements of their input resistance (R(N)) and time constant (τ₀). Based on the physiological data and on the morphological reconstruction of the labeled cells, detailed steady-state and compartmental models of VM were built and utilized to estimate the range of membrane resistivity, membrane capacitance, and cytoplasm resistivity values (R(m), C(m), and R(i), respectively) and to explore the integrative properties of these cells. VMs are relatively small cells with a simple dendritic structure. Each cell has a average of 5.3 smooth (nonspiny), short (251 μm) dendrites with a low order (2) of branching. The average soma-dendritic surface area of VMs is 9,876 μm². Electrically, VMs show remarkably linear membrane properties in the hyperpolarizing direction; they have an average R(N) of 67 ± 23 (SD) MΩ and a τ₀ of 9.4 ± 4.1 ms. Several unfavorable experimental conditions precluded the possibility of faithfully recovering ('peeling') the first equalizing time constant (τ₁) and, thereby, of estimating the electrotonic length (L(peel)) of VMs. Reconciling VM morphology with the measured R(N) and τ₀ through the models, assuming an R(i) of 70 Ω · cm and a spatially uniform R(m), yielded an R(m) estimate of 5,250 Ω · cm² and a C(m) of 1.8 μF/cm². Peeling theoretical transients produced by these models result in an L(peel) of 1.35. Because of marked differences in the length of dendrites within a single cell, this value is larger than the maximal cable length of the dendrites and is twice as long as their average cable length. The morphological and physiological data could be matched indistinguishably well if a possible soma shunt (i.e., R(m,soma) < R(m,dend)) was included in the model. Although there is no unique solution for the exact model R(m), a general conclusion regarding the integrative capabilities of VM could be drawn. As long as the model is consistent with the experimental data, the average input resistance at the dendritic terminals (R(T)) and the steady-state central (AF(T → S)) and peripheral (AF(S → T)) attenuation factors are essentially the same in the different models. With R(i) = 70 Ω · cm, we calculated R(T), AF(S → T), and AF(T → S) to be, on the average, 580 MΩ, 1.1, and 13, respectively. A new parameter, Ψ = (AF(T → S)/AF(S → T)), is introduced to characterize the asymmetry in central versus peripheral attenuation of voltages in dendritic trees. This parameter, which is estimated to be 10 in VM (with R(i) = 70 Ω · cm), serves to complement the measure (L(peel)) that represents only the peripheral 'compactness' of the tree. The integrative properties of VM critically depend on the value of R(i). Whereas increasing R(i) from 70 Ω · cm to 210 Ω · cm results in only a minor decrease in R(m) (to fit the experimental R(N)), both R(T), AF(T → S), and Ψ increased significantly (by a factor of 2, 5, and 2, respectively).