Limits...
Somato-dendritic morphology and dendritic signal transfer properties differentiate between fore- and hindlimb innervating motoneurons in the frog Rana esculenta.

Stelescu A, Sümegi J, Wéber I, Birinyi A, Wolf E - BMC Neurosci (2012)

Bottom Line: On the other hand no segregation was observed by the steady-state current transfer except under high background activity.We found size-dependent and size-independent differences in morphology and electrical structure of the limb moving motoneurons based on their spinal segmental location in frogs.Location specificity of locomotor networks is therefore partly due to segmental differences in motoneurons driving fore-, and hindlimbs.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Histology and Embryology, Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Nagyerdei krt 98, Debrecen, H-4032, Hungary.

ABSTRACT

Background: The location specific motor pattern generation properties of the spinal cord along its rostro-caudal axis have been demonstrated. However, it is still unclear that these differences are due to the different spinal interneuronal networks underlying locomotions or there are also segmental differences in motoneurons innervating different limbs. Frogs use their fore- and hindlimbs differently during jumping and swimming. Therefore we hypothesized that limb innervating motoneurons, located in the cervical and lumbar spinal cord, are different in their morphology and dendritic signal transfer properties. The test of this hypothesis what we report here.

Results: Discriminant analysis classified segmental origin of the intracellularly labeled and three-dimensionally reconstructed motoneurons 100% correctly based on twelve morphological variables. Somata of lumbar motoneurons were rounder; the dendrites had bigger total length, more branches with higher branching orders and different spatial distributions of branch points. The ventro-medial extent of cervical dendrites was bigger than in lumbar motoneurons. Computational models of the motoneurons showed that dendritic signal transfer properties were also different in the two groups of motoneurons. Whether log attenuations were higher or lower in cervical than in lumbar motoneurons depended on the proximity of dendritic input to the soma. To investigate dendritic voltage and current transfer properties imposed by dendritic architecture rather than by neuronal size we used standardized distributions of transfer variables. We introduced a novel combination of cluster analysis and homogeneity indexes to quantify segmental segregation tendencies of motoneurons based on their dendritic transfer properties. A segregation tendency of cervical and lumbar motoneurons was detected by the rates of steady-state and transient voltage-amplitude transfers from dendrites to soma at all levels of synaptic background activities, modeled by varying the specific dendritic membrane resistance. On the other hand no segregation was observed by the steady-state current transfer except under high background activity.

Conclusions: We found size-dependent and size-independent differences in morphology and electrical structure of the limb moving motoneurons based on their spinal segmental location in frogs. Location specificity of locomotor networks is therefore partly due to segmental differences in motoneurons driving fore-, and hindlimbs.

Show MeSH

Related in: MedlinePlus

Comparison of morphoelectrotonic transformations with their original geometry in (A) cervical and (B) lumbar MNs. Somatopetal log attenuations of PSPs were computed from thousands of dendritic locations per neuron and divided by the mean attenuation calculated from locations within 100 μm from the soma. Finally, these ratios (relative log attenuations) were averaged and graphed over 100 μm path distance ranges from the soma. Attenuation ratios were computed in four different models of MNs by using 1.4 MΩ neuron resistance with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (closed and open rectangles) and by 5 MΩ neuron resistance with homogeneous and inhomogeneous membranes (closed and open circles). In homogeneous membrane models Rmd was equal to Rms, in inhomogeneous models Rmd = 20000 Ωcm2 was assumed. The common specific membrane resistance for the soma and dendrites in homogeneous models and the Rms values in inhomogeneous models were defined to have neurons with 1.4 or 5 MΩ input resistance measured at the soma. Continuous linear thick line is a reference where data points would be positioned if METs cause proportional changes in size of dendrites relative to their morphological appearance. Note that many error bars, representing S.E.M.s, are too small to be visible because of the high numbers of sampling sites.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3472316&req=5

Figure 7: Comparison of morphoelectrotonic transformations with their original geometry in (A) cervical and (B) lumbar MNs. Somatopetal log attenuations of PSPs were computed from thousands of dendritic locations per neuron and divided by the mean attenuation calculated from locations within 100 μm from the soma. Finally, these ratios (relative log attenuations) were averaged and graphed over 100 μm path distance ranges from the soma. Attenuation ratios were computed in four different models of MNs by using 1.4 MΩ neuron resistance with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (closed and open rectangles) and by 5 MΩ neuron resistance with homogeneous and inhomogeneous membranes (closed and open circles). In homogeneous membrane models Rmd was equal to Rms, in inhomogeneous models Rmd = 20000 Ωcm2 was assumed. The common specific membrane resistance for the soma and dendrites in homogeneous models and the Rms values in inhomogeneous models were defined to have neurons with 1.4 or 5 MΩ input resistance measured at the soma. Continuous linear thick line is a reference where data points would be positioned if METs cause proportional changes in size of dendrites relative to their morphological appearance. Note that many error bars, representing S.E.M.s, are too small to be visible because of the high numbers of sampling sites.

Mentions: To investigate these changes further, log attenuations of PSPs to soma were determined from different regions of the dendrites located within 100 μm path distance domains from the perikaryon. Then, the computed attenuations were divided by the mean attenuation of PSPs measured from dendritic sites within 0–100 μm from the perikaryon. These relative attenuations were not linearly related to the path distances of locations where PSPs were generated indicating again a non-proportional change in size of dendrites during the METs (Figure 7). Relative log attenuations deviated more from the linear reference line in the distant regions and the size of this deviation depended on the membrane model used. Rates of log attenuations computed in a given membrane model were proved to be different in cervical (Figure 7A) and lumbar (Figure 7B) MNs. In MNs from the cervical spinal cord, the METs caused more proportional changes in the size of dendrites (data points were closer to the reference line), while in lumbar MNs the ratios of attenuations showed increasingly bigger deviations from the reference line in the more distant domains (Figure 7, see also dendrites marked by arrows in Figure 6). The biggest deviations from the proportional change were found in METs when inhomogeneous (Rms < Rmd) membrane model with 1.4 MΩ neuron input resistance was assumed.


Somato-dendritic morphology and dendritic signal transfer properties differentiate between fore- and hindlimb innervating motoneurons in the frog Rana esculenta.

Stelescu A, Sümegi J, Wéber I, Birinyi A, Wolf E - BMC Neurosci (2012)

Comparison of morphoelectrotonic transformations with their original geometry in (A) cervical and (B) lumbar MNs. Somatopetal log attenuations of PSPs were computed from thousands of dendritic locations per neuron and divided by the mean attenuation calculated from locations within 100 μm from the soma. Finally, these ratios (relative log attenuations) were averaged and graphed over 100 μm path distance ranges from the soma. Attenuation ratios were computed in four different models of MNs by using 1.4 MΩ neuron resistance with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (closed and open rectangles) and by 5 MΩ neuron resistance with homogeneous and inhomogeneous membranes (closed and open circles). In homogeneous membrane models Rmd was equal to Rms, in inhomogeneous models Rmd = 20000 Ωcm2 was assumed. The common specific membrane resistance for the soma and dendrites in homogeneous models and the Rms values in inhomogeneous models were defined to have neurons with 1.4 or 5 MΩ input resistance measured at the soma. Continuous linear thick line is a reference where data points would be positioned if METs cause proportional changes in size of dendrites relative to their morphological appearance. Note that many error bars, representing S.E.M.s, are too small to be visible because of the high numbers of sampling sites.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3472316&req=5

Figure 7: Comparison of morphoelectrotonic transformations with their original geometry in (A) cervical and (B) lumbar MNs. Somatopetal log attenuations of PSPs were computed from thousands of dendritic locations per neuron and divided by the mean attenuation calculated from locations within 100 μm from the soma. Finally, these ratios (relative log attenuations) were averaged and graphed over 100 μm path distance ranges from the soma. Attenuation ratios were computed in four different models of MNs by using 1.4 MΩ neuron resistance with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (closed and open rectangles) and by 5 MΩ neuron resistance with homogeneous and inhomogeneous membranes (closed and open circles). In homogeneous membrane models Rmd was equal to Rms, in inhomogeneous models Rmd = 20000 Ωcm2 was assumed. The common specific membrane resistance for the soma and dendrites in homogeneous models and the Rms values in inhomogeneous models were defined to have neurons with 1.4 or 5 MΩ input resistance measured at the soma. Continuous linear thick line is a reference where data points would be positioned if METs cause proportional changes in size of dendrites relative to their morphological appearance. Note that many error bars, representing S.E.M.s, are too small to be visible because of the high numbers of sampling sites.
Mentions: To investigate these changes further, log attenuations of PSPs to soma were determined from different regions of the dendrites located within 100 μm path distance domains from the perikaryon. Then, the computed attenuations were divided by the mean attenuation of PSPs measured from dendritic sites within 0–100 μm from the perikaryon. These relative attenuations were not linearly related to the path distances of locations where PSPs were generated indicating again a non-proportional change in size of dendrites during the METs (Figure 7). Relative log attenuations deviated more from the linear reference line in the distant regions and the size of this deviation depended on the membrane model used. Rates of log attenuations computed in a given membrane model were proved to be different in cervical (Figure 7A) and lumbar (Figure 7B) MNs. In MNs from the cervical spinal cord, the METs caused more proportional changes in the size of dendrites (data points were closer to the reference line), while in lumbar MNs the ratios of attenuations showed increasingly bigger deviations from the reference line in the more distant domains (Figure 7, see also dendrites marked by arrows in Figure 6). The biggest deviations from the proportional change were found in METs when inhomogeneous (Rms < Rmd) membrane model with 1.4 MΩ neuron input resistance was assumed.

Bottom Line: On the other hand no segregation was observed by the steady-state current transfer except under high background activity.We found size-dependent and size-independent differences in morphology and electrical structure of the limb moving motoneurons based on their spinal segmental location in frogs.Location specificity of locomotor networks is therefore partly due to segmental differences in motoneurons driving fore-, and hindlimbs.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Anatomy, Histology and Embryology, Faculty of Medicine, Medical and Health Science Center, University of Debrecen, Nagyerdei krt 98, Debrecen, H-4032, Hungary.

ABSTRACT

Background: The location specific motor pattern generation properties of the spinal cord along its rostro-caudal axis have been demonstrated. However, it is still unclear that these differences are due to the different spinal interneuronal networks underlying locomotions or there are also segmental differences in motoneurons innervating different limbs. Frogs use their fore- and hindlimbs differently during jumping and swimming. Therefore we hypothesized that limb innervating motoneurons, located in the cervical and lumbar spinal cord, are different in their morphology and dendritic signal transfer properties. The test of this hypothesis what we report here.

Results: Discriminant analysis classified segmental origin of the intracellularly labeled and three-dimensionally reconstructed motoneurons 100% correctly based on twelve morphological variables. Somata of lumbar motoneurons were rounder; the dendrites had bigger total length, more branches with higher branching orders and different spatial distributions of branch points. The ventro-medial extent of cervical dendrites was bigger than in lumbar motoneurons. Computational models of the motoneurons showed that dendritic signal transfer properties were also different in the two groups of motoneurons. Whether log attenuations were higher or lower in cervical than in lumbar motoneurons depended on the proximity of dendritic input to the soma. To investigate dendritic voltage and current transfer properties imposed by dendritic architecture rather than by neuronal size we used standardized distributions of transfer variables. We introduced a novel combination of cluster analysis and homogeneity indexes to quantify segmental segregation tendencies of motoneurons based on their dendritic transfer properties. A segregation tendency of cervical and lumbar motoneurons was detected by the rates of steady-state and transient voltage-amplitude transfers from dendrites to soma at all levels of synaptic background activities, modeled by varying the specific dendritic membrane resistance. On the other hand no segregation was observed by the steady-state current transfer except under high background activity.

Conclusions: We found size-dependent and size-independent differences in morphology and electrical structure of the limb moving motoneurons based on their spinal segmental location in frogs. Location specificity of locomotor networks is therefore partly due to segmental differences in motoneurons driving fore-, and hindlimbs.

Show MeSH
Related in: MedlinePlus