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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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Polar histograms showing angular distributions of dendritic lengths projected to the transverse plane. Full circle around somata (S) was divided into 40 degree angle intervals starting with the dorsal direction (0°), the total lengths of dendritic branches were measured within these intervals and averaged over MNs within the same part of the cord. Mean dendritic lengths were represented on a relative scale by the length of a line drawn from the soma in the given direction and finally end points of these lines were interconnected (gray line for the cervical MNs and black line for lumbar MNs). The direction with the longest dendritic length was taken as 100% for the lumbar and cervical MNs separately. Ventromedial (VM) direction (120–160°), where significant segmental difference in angular distributions of dendrites was detected (Mann–Whitney-test, p < 0.05) is shaded in gray.
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Figure 5: Polar histograms showing angular distributions of dendritic lengths projected to the transverse plane. Full circle around somata (S) was divided into 40 degree angle intervals starting with the dorsal direction (0°), the total lengths of dendritic branches were measured within these intervals and averaged over MNs within the same part of the cord. Mean dendritic lengths were represented on a relative scale by the length of a line drawn from the soma in the given direction and finally end points of these lines were interconnected (gray line for the cervical MNs and black line for lumbar MNs). The direction with the longest dendritic length was taken as 100% for the lumbar and cervical MNs separately. Ventromedial (VM) direction (120–160°), where significant segmental difference in angular distributions of dendrites was detected (Mann–Whitney-test, p < 0.05) is shaded in gray.

Mentions: Here we compared orientation of MN dendrites in the lumbar and cervical levels of the cord. Polar histograms were created (Figure 5) to show average dendritic lengths within equal angle domains around the perikarya of MNs in the transverse plane of the spinal cord. To identify the anatomical directions where lengths of dendritic projections differentiated significantly between cervical and lumbar MNs pair-wise comparisons were used. We found that ventro-medial dendritic extension was significantly bigger in the cervical MNs (Mann–Whitney test, p < 0.05). This is well correlated with the anatomical finding that the ventro-medial region of dendritic trees in cervical MNs is the exclusive terminal zone for tecto-spinal pathways in frogs and this type of connection is not received by lumbar MNs [44].


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)

Polar histograms showing angular distributions of dendritic lengths projected to the transverse plane. Full circle around somata (S) was divided into 40 degree angle intervals starting with the dorsal direction (0°), the total lengths of dendritic branches were measured within these intervals and averaged over MNs within the same part of the cord. Mean dendritic lengths were represented on a relative scale by the length of a line drawn from the soma in the given direction and finally end points of these lines were interconnected (gray line for the cervical MNs and black line for lumbar MNs). The direction with the longest dendritic length was taken as 100% for the lumbar and cervical MNs separately. Ventromedial (VM) direction (120–160°), where significant segmental difference in angular distributions of dendrites was detected (Mann–Whitney-test, p < 0.05) is shaded in gray.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Polar histograms showing angular distributions of dendritic lengths projected to the transverse plane. Full circle around somata (S) was divided into 40 degree angle intervals starting with the dorsal direction (0°), the total lengths of dendritic branches were measured within these intervals and averaged over MNs within the same part of the cord. Mean dendritic lengths were represented on a relative scale by the length of a line drawn from the soma in the given direction and finally end points of these lines were interconnected (gray line for the cervical MNs and black line for lumbar MNs). The direction with the longest dendritic length was taken as 100% for the lumbar and cervical MNs separately. Ventromedial (VM) direction (120–160°), where significant segmental difference in angular distributions of dendrites was detected (Mann–Whitney-test, p < 0.05) is shaded in gray.
Mentions: Here we compared orientation of MN dendrites in the lumbar and cervical levels of the cord. Polar histograms were created (Figure 5) to show average dendritic lengths within equal angle domains around the perikarya of MNs in the transverse plane of the spinal cord. To identify the anatomical directions where lengths of dendritic projections differentiated significantly between cervical and lumbar MNs pair-wise comparisons were used. We found that ventro-medial dendritic extension was significantly bigger in the cervical MNs (Mann–Whitney test, p < 0.05). This is well correlated with the anatomical finding that the ventro-medial region of dendritic trees in cervical MNs is the exclusive terminal zone for tecto-spinal pathways in frogs and this type of connection is not received by lumbar MNs [44].

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