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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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Voltage and current transfers in steady-state. Box plots show 10th, 25th, 50th, 75th and 90th percentiles of standardized and area weighted voltage- (A) and current transfers (D) in steady-state measured from dendritic points to the soma in limb moving MNs in the cervical (shaded boxes) and lumbar (open boxes) segments. Higher and lower percentiles were weighted relative to the median (50th percentile) and used as descriptors for cluster analysis of MNs. The 10th and 90th as well as the 25th and 75th percentiles are shown by the wings and by the borders of boxes respectively, the median is marked by the line within the box (see insert). Dendrograms show segmental segregation tendencies between the cervical and lumbar MNs based on voltage and current transfer properties under high (voltage: part B, current: part E) and low (voltage: part C, current: part F) background synaptic activities. Different levels of synaptic background activities were modeled by varying the specific dendritic membrane resistance (Rmd). High activity: Rmd = 5000 Ωcm2 and low activity: Rmd = 50000 Ωcm2. In cluster analyses shown, the Ward’s method was used and the weighting factors for percentiles were: 0.2 for the 10th and 90th percentiles and 0.8 for the 25th and 75th percentiles. MN labels starting with letters C and L stand for the cervical and lumbar neurons respectively.
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Figure 9: Voltage and current transfers in steady-state. Box plots show 10th, 25th, 50th, 75th and 90th percentiles of standardized and area weighted voltage- (A) and current transfers (D) in steady-state measured from dendritic points to the soma in limb moving MNs in the cervical (shaded boxes) and lumbar (open boxes) segments. Higher and lower percentiles were weighted relative to the median (50th percentile) and used as descriptors for cluster analysis of MNs. The 10th and 90th as well as the 25th and 75th percentiles are shown by the wings and by the borders of boxes respectively, the median is marked by the line within the box (see insert). Dendrograms show segmental segregation tendencies between the cervical and lumbar MNs based on voltage and current transfer properties under high (voltage: part B, current: part E) and low (voltage: part C, current: part F) background synaptic activities. Different levels of synaptic background activities were modeled by varying the specific dendritic membrane resistance (Rmd). High activity: Rmd = 5000 Ωcm2 and low activity: Rmd = 50000 Ωcm2. In cluster analyses shown, the Ward’s method was used and the weighting factors for percentiles were: 0.2 for the 10th and 90th percentiles and 0.8 for the 25th and 75th percentiles. MN labels starting with letters C and L stand for the cervical and lumbar neurons respectively.

Mentions: To focus on such structural rather than size-related features of dendrites, we used distributions of standardized and area weighted voltage and current transfer values [34]. The data processing is exemplified in Figure 1 by the steady-state currents transfers. The starting point is the set of transfer values computed between the mid-points of each dendritic compartment and the soma. The frequency distribution of these transfers (Figure 1A) gives equal weight to each measurement (compartment). However, transfers measured from larger compartments approximate attenuations for more synapses since the number of synapses received by a dendritic compartment is directly proportional to the area of the compartment [37]. To take this into account, in the second step, the raw measurements of transfers were area weighted (Figure 1B) to give proportionally bigger weight to compartments with larger surface area. Finally, area weighted distributions of signal transfers were standardized (Figure 1C) to create distributions with shapes, characteristic to signal transfer properties of neurons independently of their variable size. The shapes of these standardized distributions were described by their 10th, 25th, 50th, 75th and 90th percentiles (these were graphed as box plots in Figures 9 and 10). The percentiles were then weighted relative to the median and used as descriptors of the standardized distributions in the cluster analysis to reveal grouping tendencies of cervical and lumbar MNs. While cluster analysis is generally considered as an objective way to reveal grouping of objects, the method suffers from the lack of criteria on how the similarity level should be chosen where cluster formations are analyzed. Here, we decided to study cluster formations at the end of the hierarchical cluster analysis, when the two biggest clusters appear before including all MNs in a single group (last order clustering, Figure 2, see also Methods). The advantage of this method was the determination of the similarity level by the dendrograms themselves and not by the investigator who carried out the analysis.


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)

Voltage and current transfers in steady-state. Box plots show 10th, 25th, 50th, 75th and 90th percentiles of standardized and area weighted voltage- (A) and current transfers (D) in steady-state measured from dendritic points to the soma in limb moving MNs in the cervical (shaded boxes) and lumbar (open boxes) segments. Higher and lower percentiles were weighted relative to the median (50th percentile) and used as descriptors for cluster analysis of MNs. The 10th and 90th as well as the 25th and 75th percentiles are shown by the wings and by the borders of boxes respectively, the median is marked by the line within the box (see insert). Dendrograms show segmental segregation tendencies between the cervical and lumbar MNs based on voltage and current transfer properties under high (voltage: part B, current: part E) and low (voltage: part C, current: part F) background synaptic activities. Different levels of synaptic background activities were modeled by varying the specific dendritic membrane resistance (Rmd). High activity: Rmd = 5000 Ωcm2 and low activity: Rmd = 50000 Ωcm2. In cluster analyses shown, the Ward’s method was used and the weighting factors for percentiles were: 0.2 for the 10th and 90th percentiles and 0.8 for the 25th and 75th percentiles. MN labels starting with letters C and L stand for the cervical and lumbar neurons respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 9: Voltage and current transfers in steady-state. Box plots show 10th, 25th, 50th, 75th and 90th percentiles of standardized and area weighted voltage- (A) and current transfers (D) in steady-state measured from dendritic points to the soma in limb moving MNs in the cervical (shaded boxes) and lumbar (open boxes) segments. Higher and lower percentiles were weighted relative to the median (50th percentile) and used as descriptors for cluster analysis of MNs. The 10th and 90th as well as the 25th and 75th percentiles are shown by the wings and by the borders of boxes respectively, the median is marked by the line within the box (see insert). Dendrograms show segmental segregation tendencies between the cervical and lumbar MNs based on voltage and current transfer properties under high (voltage: part B, current: part E) and low (voltage: part C, current: part F) background synaptic activities. Different levels of synaptic background activities were modeled by varying the specific dendritic membrane resistance (Rmd). High activity: Rmd = 5000 Ωcm2 and low activity: Rmd = 50000 Ωcm2. In cluster analyses shown, the Ward’s method was used and the weighting factors for percentiles were: 0.2 for the 10th and 90th percentiles and 0.8 for the 25th and 75th percentiles. MN labels starting with letters C and L stand for the cervical and lumbar neurons respectively.
Mentions: To focus on such structural rather than size-related features of dendrites, we used distributions of standardized and area weighted voltage and current transfer values [34]. The data processing is exemplified in Figure 1 by the steady-state currents transfers. The starting point is the set of transfer values computed between the mid-points of each dendritic compartment and the soma. The frequency distribution of these transfers (Figure 1A) gives equal weight to each measurement (compartment). However, transfers measured from larger compartments approximate attenuations for more synapses since the number of synapses received by a dendritic compartment is directly proportional to the area of the compartment [37]. To take this into account, in the second step, the raw measurements of transfers were area weighted (Figure 1B) to give proportionally bigger weight to compartments with larger surface area. Finally, area weighted distributions of signal transfers were standardized (Figure 1C) to create distributions with shapes, characteristic to signal transfer properties of neurons independently of their variable size. The shapes of these standardized distributions were described by their 10th, 25th, 50th, 75th and 90th percentiles (these were graphed as box plots in Figures 9 and 10). The percentiles were then weighted relative to the median and used as descriptors of the standardized distributions in the cluster analysis to reveal grouping tendencies of cervical and lumbar MNs. While cluster analysis is generally considered as an objective way to reveal grouping of objects, the method suffers from the lack of criteria on how the similarity level should be chosen where cluster formations are analyzed. Here, we decided to study cluster formations at the end of the hierarchical cluster analysis, when the two biggest clusters appear before including all MNs in a single group (last order clustering, Figure 2, see also Methods). The advantage of this method was the determination of the similarity level by the dendrograms themselves and not by the investigator who carried out the analysis.

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