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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.

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Comparison of somatopetal log attenuations of postsynaptic potentials. Attenuations of PSPs were computed from dendritic locations and averaged within 100 μm path distance ranges from the soma. Homogeneous (Rms = Rmd, part A and B) and inhomogeneous (Rms < Rmd, part C and D) soma-dendrite membrane models were used with 1.4 MΩ (A and C) and 5.0 MΩ (B and D) neuron resistances, where Rms and Rmd values were defined as described in the legend of Figure 7. A characteristic 1400–1500 μm distance, the limit of distance domains where attenuations in cervical (closed circles) and lumbar MNs (open circles) were significantly different were marked by vertical dotted lines. Many error bars are not visible due to their very low values.
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Figure 8: Comparison of somatopetal log attenuations of postsynaptic potentials. Attenuations of PSPs were computed from dendritic locations and averaged within 100 μm path distance ranges from the soma. Homogeneous (Rms = Rmd, part A and B) and inhomogeneous (Rms < Rmd, part C and D) soma-dendrite membrane models were used with 1.4 MΩ (A and C) and 5.0 MΩ (B and D) neuron resistances, where Rms and Rmd values were defined as described in the legend of Figure 7. A characteristic 1400–1500 μm distance, the limit of distance domains where attenuations in cervical (closed circles) and lumbar MNs (open circles) were significantly different were marked by vertical dotted lines. Many error bars are not visible due to their very low values.

Mentions: The mean somatopetal log attenuations of PSPs were determined as a function of path distance from the soma in different membrane models of the cervical and lumbar MNs (Figure 8). Generally, PSPs attenuated differently (Mann–Whitney test, p < 10−6) from the same geometrical distance in lumbar and in cervical MNs both in the homogeneous (Rms = Rmd), Figure 8A–B) and in the inhomogeneous (Rms < Rmd, Figure 8C–D) soma-dendritic membrane models. If the distance of the site of PSP initiation was closer than 1400–1500 μm to the soma then PSPs attenuated more in the lumbar MNs, while PSPs generated farther than this characteristic distance attenuated less in lumbar MNs. The characteristic distance separating the two distance domains from where PSPs attenuated differently was virtually independent of the size of inhomogeneity of the soma-dendritic membrane and the input resistance of neurons. Differences between the rates of log attenuations in cervical and lumbar MNs were reduced when inhomogeneous rather than homogeneous soma-dendritic membrane was assumed. However, even small but significant differences measured on a logarithmic scale by log attenuations may be translated to considerably divergent voltage-time integrals on the somata of segmentally different MNs.


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 somatopetal log attenuations of postsynaptic potentials. Attenuations of PSPs were computed from dendritic locations and averaged within 100 μm path distance ranges from the soma. Homogeneous (Rms = Rmd, part A and B) and inhomogeneous (Rms < Rmd, part C and D) soma-dendrite membrane models were used with 1.4 MΩ (A and C) and 5.0 MΩ (B and D) neuron resistances, where Rms and Rmd values were defined as described in the legend of Figure 7. A characteristic 1400–1500 μm distance, the limit of distance domains where attenuations in cervical (closed circles) and lumbar MNs (open circles) were significantly different were marked by vertical dotted lines. Many error bars are not visible due to their very low values.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 8: Comparison of somatopetal log attenuations of postsynaptic potentials. Attenuations of PSPs were computed from dendritic locations and averaged within 100 μm path distance ranges from the soma. Homogeneous (Rms = Rmd, part A and B) and inhomogeneous (Rms < Rmd, part C and D) soma-dendrite membrane models were used with 1.4 MΩ (A and C) and 5.0 MΩ (B and D) neuron resistances, where Rms and Rmd values were defined as described in the legend of Figure 7. A characteristic 1400–1500 μm distance, the limit of distance domains where attenuations in cervical (closed circles) and lumbar MNs (open circles) were significantly different were marked by vertical dotted lines. Many error bars are not visible due to their very low values.
Mentions: The mean somatopetal log attenuations of PSPs were determined as a function of path distance from the soma in different membrane models of the cervical and lumbar MNs (Figure 8). Generally, PSPs attenuated differently (Mann–Whitney test, p < 10−6) from the same geometrical distance in lumbar and in cervical MNs both in the homogeneous (Rms = Rmd), Figure 8A–B) and in the inhomogeneous (Rms < Rmd, Figure 8C–D) soma-dendritic membrane models. If the distance of the site of PSP initiation was closer than 1400–1500 μm to the soma then PSPs attenuated more in the lumbar MNs, while PSPs generated farther than this characteristic distance attenuated less in lumbar MNs. The characteristic distance separating the two distance domains from where PSPs attenuated differently was virtually independent of the size of inhomogeneity of the soma-dendritic membrane and the input resistance of neurons. Differences between the rates of log attenuations in cervical and lumbar MNs were reduced when inhomogeneous rather than homogeneous soma-dendritic membrane was assumed. However, even small but significant differences measured on a logarithmic scale by log attenuations may be translated to considerably divergent voltage-time integrals on the somata of segmentally different MNs.

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