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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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Camera lucida drawings of dendritic trees of fore- and hindlimb moving motoneurons (MNs) of frogs. Neurons are from the 3rd cervical and the 8th or 9th lumbar segments as seen in the transverse plane of the spinal cord. Drawings of MNs were superimposed with the contours of spinal cord to show locations of somata and direction and extent of dendrites. Dashed lines mark the border of white and gray matters. Scale bars are 100 μm. Part of this Figure was reprinted from [10] and [11] with permissions of the publishers Elsevier and John Wiley & Sons.
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Figure 3: Camera lucida drawings of dendritic trees of fore- and hindlimb moving motoneurons (MNs) of frogs. Neurons are from the 3rd cervical and the 8th or 9th lumbar segments as seen in the transverse plane of the spinal cord. Drawings of MNs were superimposed with the contours of spinal cord to show locations of somata and direction and extent of dendrites. Dashed lines mark the border of white and gray matters. Scale bars are 100 μm. Part of this Figure was reprinted from [10] and [11] with permissions of the publishers Elsevier and John Wiley & Sons.

Mentions: The purpose of this study was to investigate differences between alpha motoneurons (MNs) located in the cervical and lumbar enlargements of the frog that innervate the muscles of forelimbs and hindlimbs. These MNs had ellipsoid or fusiform perikarya in the lateral area of the ventral horn. The dendritic arborization of these MNs could be divided into a dorsomedial, dorsal and lateral dendritic arrays with many dendrites extending to the lateral funiculus of the white matter. The lateral dendrites extended to the border of spinal cord where they formed a subpial meshwork (Figure 3), characteristic to the frog spinal cord [8,10]. We used this latter criterion to justify that dendrites were fully labeled and the limb-innervating type of MNs was validated by using the features described above (Figure 3).


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)

Camera lucida drawings of dendritic trees of fore- and hindlimb moving motoneurons (MNs) of frogs. Neurons are from the 3rd cervical and the 8th or 9th lumbar segments as seen in the transverse plane of the spinal cord. Drawings of MNs were superimposed with the contours of spinal cord to show locations of somata and direction and extent of dendrites. Dashed lines mark the border of white and gray matters. Scale bars are 100 μm. Part of this Figure was reprinted from [10] and [11] with permissions of the publishers Elsevier and John Wiley & Sons.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Camera lucida drawings of dendritic trees of fore- and hindlimb moving motoneurons (MNs) of frogs. Neurons are from the 3rd cervical and the 8th or 9th lumbar segments as seen in the transverse plane of the spinal cord. Drawings of MNs were superimposed with the contours of spinal cord to show locations of somata and direction and extent of dendrites. Dashed lines mark the border of white and gray matters. Scale bars are 100 μm. Part of this Figure was reprinted from [10] and [11] with permissions of the publishers Elsevier and John Wiley & Sons.
Mentions: The purpose of this study was to investigate differences between alpha motoneurons (MNs) located in the cervical and lumbar enlargements of the frog that innervate the muscles of forelimbs and hindlimbs. These MNs had ellipsoid or fusiform perikarya in the lateral area of the ventral horn. The dendritic arborization of these MNs could be divided into a dorsomedial, dorsal and lateral dendritic arrays with many dendrites extending to the lateral funiculus of the white matter. The lateral dendrites extended to the border of spinal cord where they formed a subpial meshwork (Figure 3), characteristic to the frog spinal cord [8,10]. We used this latter criterion to justify that dendrites were fully labeled and the limb-innervating type of MNs was validated by using the features described above (Figure 3).

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