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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

Grouping tendencies of MNs based on steady-state voltage- and current transfers (open and closed triangles). ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively. To reveal grouping tendencies cluster analysis was used with the Pair group and Ward’s methods (see horizontal labels starting with ‘pg’ and ‘wm’) with differently weighted (‘fact1’ and ‘fact2’) descriptors. The five descriptors were the 10th, 25th, 50th, 75th, and 90th percentiles of standardized and area weighted distributions of voltage and current transfers between dendritic points and the soma. The two sets of weighting factors of percentiles (‘fact1’ and ‘fact2’) were as follows: In factor set 1, the 10th and 90th percentiles were weighted by 0.2 and the 25th and 75th percentiles by 0.8. In factor set 2, the weighting factors were 0.33 for the 10th and 90th percentiles and 0.67 for the 25th and 75th percentiles. In both sets of weighting factors the weight was 1 for the 50th percentile. In cluster analyses the Euclidian distances were used. Homogeneity indexes, last order clustering index (A) and Peterson’s index (B), were used to measure segmental homogeneities of MNs within last order clusters, which reflect segregation of cervical and lumbar MNs between the clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark the levels of homogeneity indexes below which segmental separation of MNs by their voltage and current transfer properties is significant.
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Figure 11: Grouping tendencies of MNs based on steady-state voltage- and current transfers (open and closed triangles). ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively. To reveal grouping tendencies cluster analysis was used with the Pair group and Ward’s methods (see horizontal labels starting with ‘pg’ and ‘wm’) with differently weighted (‘fact1’ and ‘fact2’) descriptors. The five descriptors were the 10th, 25th, 50th, 75th, and 90th percentiles of standardized and area weighted distributions of voltage and current transfers between dendritic points and the soma. The two sets of weighting factors of percentiles (‘fact1’ and ‘fact2’) were as follows: In factor set 1, the 10th and 90th percentiles were weighted by 0.2 and the 25th and 75th percentiles by 0.8. In factor set 2, the weighting factors were 0.33 for the 10th and 90th percentiles and 0.67 for the 25th and 75th percentiles. In both sets of weighting factors the weight was 1 for the 50th percentile. In cluster analyses the Euclidian distances were used. Homogeneity indexes, last order clustering index (A) and Peterson’s index (B), were used to measure segmental homogeneities of MNs within last order clusters, which reflect segregation of cervical and lumbar MNs between the clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark the levels of homogeneity indexes below which segmental separation of MNs by their voltage and current transfer properties is significant.

Mentions: By using somatopetal voltage transfers, our first observation was the higher variabilities for all, except the 90th percentiles of distributions for the lumbar MNs (F-test, p < 0.02) and the generally shifted nature of percentiles relative to those of the cervical MN group (Figure 9A). Indeed, hierarchical cluster analysis proved segregation tendency of the cervical and lumbar MNs. Under high background synaptic activity one of the last order clusters was homogeneous and contained five lumbar MNs without any cervical ones, while the other cluster contained all cervical neurons along with three lumbar ones (Figure 9B). The tendency of segregation was present at all intensities of synaptic background activity but segregation was a bit weaker if synaptic activity was low (Figure 9C). In this case the two last order clusters contained lumbar and cervical MNs in ratios of 5:1 and 3:7. The significance in the tendency of segmental segregation was tested by comparing the actual homogeneity indexes of last order clusters (last order clustering index and Peterson’s index) to the mean indexes calculated for clusters formed when segmental origins of MNs were artificially randomized. In all of these comparisons, indexes remained below their critical values and cervical and lumbar MNs were proved to be segmentally different (Figure 11A, B, one sample t-test, p < 10−18) in their steady-state voltage transfer properties. These segmental differences between MNs were detected at all levels of background synaptic activities with some tendency of MNs to get more similar with the decrease of background activity.


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)

Grouping tendencies of MNs based on steady-state voltage- and current transfers (open and closed triangles). ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively. To reveal grouping tendencies cluster analysis was used with the Pair group and Ward’s methods (see horizontal labels starting with ‘pg’ and ‘wm’) with differently weighted (‘fact1’ and ‘fact2’) descriptors. The five descriptors were the 10th, 25th, 50th, 75th, and 90th percentiles of standardized and area weighted distributions of voltage and current transfers between dendritic points and the soma. The two sets of weighting factors of percentiles (‘fact1’ and ‘fact2’) were as follows: In factor set 1, the 10th and 90th percentiles were weighted by 0.2 and the 25th and 75th percentiles by 0.8. In factor set 2, the weighting factors were 0.33 for the 10th and 90th percentiles and 0.67 for the 25th and 75th percentiles. In both sets of weighting factors the weight was 1 for the 50th percentile. In cluster analyses the Euclidian distances were used. Homogeneity indexes, last order clustering index (A) and Peterson’s index (B), were used to measure segmental homogeneities of MNs within last order clusters, which reflect segregation of cervical and lumbar MNs between the clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark the levels of homogeneity indexes below which segmental separation of MNs by their voltage and current transfer properties is significant.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 11: Grouping tendencies of MNs based on steady-state voltage- and current transfers (open and closed triangles). ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively. To reveal grouping tendencies cluster analysis was used with the Pair group and Ward’s methods (see horizontal labels starting with ‘pg’ and ‘wm’) with differently weighted (‘fact1’ and ‘fact2’) descriptors. The five descriptors were the 10th, 25th, 50th, 75th, and 90th percentiles of standardized and area weighted distributions of voltage and current transfers between dendritic points and the soma. The two sets of weighting factors of percentiles (‘fact1’ and ‘fact2’) were as follows: In factor set 1, the 10th and 90th percentiles were weighted by 0.2 and the 25th and 75th percentiles by 0.8. In factor set 2, the weighting factors were 0.33 for the 10th and 90th percentiles and 0.67 for the 25th and 75th percentiles. In both sets of weighting factors the weight was 1 for the 50th percentile. In cluster analyses the Euclidian distances were used. Homogeneity indexes, last order clustering index (A) and Peterson’s index (B), were used to measure segmental homogeneities of MNs within last order clusters, which reflect segregation of cervical and lumbar MNs between the clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark the levels of homogeneity indexes below which segmental separation of MNs by their voltage and current transfer properties is significant.
Mentions: By using somatopetal voltage transfers, our first observation was the higher variabilities for all, except the 90th percentiles of distributions for the lumbar MNs (F-test, p < 0.02) and the generally shifted nature of percentiles relative to those of the cervical MN group (Figure 9A). Indeed, hierarchical cluster analysis proved segregation tendency of the cervical and lumbar MNs. Under high background synaptic activity one of the last order clusters was homogeneous and contained five lumbar MNs without any cervical ones, while the other cluster contained all cervical neurons along with three lumbar ones (Figure 9B). The tendency of segregation was present at all intensities of synaptic background activity but segregation was a bit weaker if synaptic activity was low (Figure 9C). In this case the two last order clusters contained lumbar and cervical MNs in ratios of 5:1 and 3:7. The significance in the tendency of segmental segregation was tested by comparing the actual homogeneity indexes of last order clusters (last order clustering index and Peterson’s index) to the mean indexes calculated for clusters formed when segmental origins of MNs were artificially randomized. In all of these comparisons, indexes remained below their critical values and cervical and lumbar MNs were proved to be segmentally different (Figure 11A, B, one sample t-test, p < 10−18) in their steady-state voltage transfer properties. These segmental differences between MNs were detected at all levels of background synaptic activities with some tendency of MNs to get more similar with the decrease of background activity.

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