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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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Segregation of cervical and lumbar limb moving motoneurons based on somatopetal propagation of voltage transients. 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. These descriptors were the standardized and area weighted percentiles of somatic to dendritic ratios of peak potentials (open triangles), half-widths (closed circles) and rise times (open circles) of PSPs to quantify the changes in shape of voltage transients generated by conductance changes according to an α-function (gmax = 2 nS, tmax = 1.5 ms). Last order clustering index (A) and Peterson’s homogeneity index (B) were used to measure homogeneities within last order clusters, which reflect segregation of cervical and lumbar MNs between these clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark levels of homogeneities below which separation of MNs is significant. ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively.
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Figure 12: Segregation of cervical and lumbar limb moving motoneurons based on somatopetal propagation of voltage transients. 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. These descriptors were the standardized and area weighted percentiles of somatic to dendritic ratios of peak potentials (open triangles), half-widths (closed circles) and rise times (open circles) of PSPs to quantify the changes in shape of voltage transients generated by conductance changes according to an α-function (gmax = 2 nS, tmax = 1.5 ms). Last order clustering index (A) and Peterson’s homogeneity index (B) were used to measure homogeneities within last order clusters, which reflect segregation of cervical and lumbar MNs between these clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark levels of homogeneities below which separation of MNs is significant. ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively.

Mentions: The two last order clusters showed significant segmental homogeneity in the origin of MNs they contained (Figure 10D) when cluster analysis was based on somatic to dendritic amplitudes of voltage transients. One of the last order clusters was purely homogeneous and contained five lumbar MNs while the other accommodated cervical and lumbar MNs in 8:3 ratio. The homogeneity indexes of these last order clusters were significantly lower (one sample t-test, p < 0.0005) than those calculated for clusters when segmental origin of MNs was artificially randomized (open triangles in Figure 12A, B). Consequently, there was a significant segmental segregation tendency between the cervical and lumbar MNs based on the attenuation of transient EPSP amplitudes. This tendency was present at all intensities of synaptic 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)

Segregation of cervical and lumbar limb moving motoneurons based on somatopetal propagation of voltage transients. 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. These descriptors were the standardized and area weighted percentiles of somatic to dendritic ratios of peak potentials (open triangles), half-widths (closed circles) and rise times (open circles) of PSPs to quantify the changes in shape of voltage transients generated by conductance changes according to an α-function (gmax = 2 nS, tmax = 1.5 ms). Last order clustering index (A) and Peterson’s homogeneity index (B) were used to measure homogeneities within last order clusters, which reflect segregation of cervical and lumbar MNs between these clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark levels of homogeneities below which separation of MNs is significant. ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 12: Segregation of cervical and lumbar limb moving motoneurons based on somatopetal propagation of voltage transients. 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. These descriptors were the standardized and area weighted percentiles of somatic to dendritic ratios of peak potentials (open triangles), half-widths (closed circles) and rise times (open circles) of PSPs to quantify the changes in shape of voltage transients generated by conductance changes according to an α-function (gmax = 2 nS, tmax = 1.5 ms). Last order clustering index (A) and Peterson’s homogeneity index (B) were used to measure homogeneities within last order clusters, which reflect segregation of cervical and lumbar MNs between these clusters. Homogeneity indexes with values closer to one indicate higher similarity (poorer segregation) of cervical and lumbar MNs. Continuous horizontal lines mark levels of homogeneities below which separation of MNs is significant. ‘High’, ‘Medium’, and ‘Low’ levels of synaptic background activities on dendrites were modeled by 5000, 20000 and 50000 Ωcm2 specific dendritic membrane resistivities respectively.
Mentions: The two last order clusters showed significant segmental homogeneity in the origin of MNs they contained (Figure 10D) when cluster analysis was based on somatic to dendritic amplitudes of voltage transients. One of the last order clusters was purely homogeneous and contained five lumbar MNs while the other accommodated cervical and lumbar MNs in 8:3 ratio. The homogeneity indexes of these last order clusters were significantly lower (one sample t-test, p < 0.0005) than those calculated for clusters when segmental origin of MNs was artificially randomized (open triangles in Figure 12A, B). Consequently, there was a significant segmental segregation tendency between the cervical and lumbar MNs based on the attenuation of transient EPSP amplitudes. This tendency was present at all intensities of synaptic 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