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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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Related in: MedlinePlus

Spatial distributions of branch points in dendritic trees of limb moving MNs. Distances of branch points were measured along dendritic paths from the soma. Closed and open circles stand for the cervical and lumbar MNs respectively. Both the mean total numbers and the distributions of branch points are significantly different (Mann–Whitney test, p < 0.005; Wilcoxon test, p < 0.0005) in MNs of the cervical and lumbar parts of the frog spinal cord.
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Figure 4: Spatial distributions of branch points in dendritic trees of limb moving MNs. Distances of branch points were measured along dendritic paths from the soma. Closed and open circles stand for the cervical and lumbar MNs respectively. Both the mean total numbers and the distributions of branch points are significantly different (Mann–Whitney test, p < 0.005; Wilcoxon test, p < 0.0005) in MNs of the cervical and lumbar parts of the frog spinal cord.

Mentions: The total number of branch points was more numerous in lumbar MNs than in MNs of the cervical part of the spinal cord (101 ± 18.9 and 59 ± 4.8 in lumbar and cervical MNs respectively, Mann–Whitney test, p < 0.005). The distributions of branch points over different path distance domains were also different (Wilcoxon test, p < 0.0005, Figure 4). In the proximal region (closer than 200 μm to the soma) the numbers of branch points were the same. The biggest difference was found at 200–300 μm distance from the soma, where the distribution curves peaked for MNs of both parts of the spinal cord. Beyond 300 μm, the frequency of branch points showed a steeper decrease with distance in cervical MNs. Dityatev et al. [42] found a similar relation between cervical and lumbar MNs for the probability of bifurcation in the function of branch order.


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)

Spatial distributions of branch points in dendritic trees of limb moving MNs. Distances of branch points were measured along dendritic paths from the soma. Closed and open circles stand for the cervical and lumbar MNs respectively. Both the mean total numbers and the distributions of branch points are significantly different (Mann–Whitney test, p < 0.005; Wilcoxon test, p < 0.0005) in MNs of the cervical and lumbar parts of the frog spinal cord.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Spatial distributions of branch points in dendritic trees of limb moving MNs. Distances of branch points were measured along dendritic paths from the soma. Closed and open circles stand for the cervical and lumbar MNs respectively. Both the mean total numbers and the distributions of branch points are significantly different (Mann–Whitney test, p < 0.005; Wilcoxon test, p < 0.0005) in MNs of the cervical and lumbar parts of the frog spinal cord.
Mentions: The total number of branch points was more numerous in lumbar MNs than in MNs of the cervical part of the spinal cord (101 ± 18.9 and 59 ± 4.8 in lumbar and cervical MNs respectively, Mann–Whitney test, p < 0.005). The distributions of branch points over different path distance domains were also different (Wilcoxon test, p < 0.0005, Figure 4). In the proximal region (closer than 200 μm to the soma) the numbers of branch points were the same. The biggest difference was found at 200–300 μm distance from the soma, where the distribution curves peaked for MNs of both parts of the spinal cord. Beyond 300 μm, the frequency of branch points showed a steeper decrease with distance in cervical MNs. Dityatev et al. [42] found a similar relation between cervical and lumbar MNs for the probability of bifurcation in the function of branch order.

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