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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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Dendritic morphology and morphoelectrotonic transforms of a cervical motoneuron. Morphology (A) and METs (B) and (C) of the same MN (C-167) with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendrite membranes constrained by the physiological 5 MΩ somatic input resistance of the MN for both METs. Arrows 1 and 2 point to homologous proximal (red) and distal (green) dendritic branches where changes during METs are visibly non-proportional to their geometrical sizes (for quantitative analysis see body text). Arrows labeled by S point to the center of the soma (its entire shape is not shown in the figures). D-dorsal, V-ventral, M-medial, L-lateral directions. Note the different size of the MET with our choice of the physiologically constrained pair of Rms-Rmd values in the inhomogeneous soma-dendritic membrane (C) relative to the MET of the same MN with homogeneous membrane (B) drawn to a common scale of space constants. Both METs show attenuations of somatopetal PSP propagation (‘Vin mode’ in NEURON) at DC input (frequency = 0 Hz), recording electrode was at mid-soma, stimulating electrode was at mid-points of dendritic compartments. Dendritic and somatic specific membrane resistances (Rmd and Rms) were equally 8348 Ωcm2 for the homogeneous soma-dendritic membrane, while for the MET with inhomogeneous membrane Rmd and Rms were 20000 and 1046 Ωcm2 respectively. With these Rms and Rmd values the somatic input resistance was 5 MΩ in both membrane models of the MN.
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Figure 6: Dendritic morphology and morphoelectrotonic transforms of a cervical motoneuron. Morphology (A) and METs (B) and (C) of the same MN (C-167) with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendrite membranes constrained by the physiological 5 MΩ somatic input resistance of the MN for both METs. Arrows 1 and 2 point to homologous proximal (red) and distal (green) dendritic branches where changes during METs are visibly non-proportional to their geometrical sizes (for quantitative analysis see body text). Arrows labeled by S point to the center of the soma (its entire shape is not shown in the figures). D-dorsal, V-ventral, M-medial, L-lateral directions. Note the different size of the MET with our choice of the physiologically constrained pair of Rms-Rmd values in the inhomogeneous soma-dendritic membrane (C) relative to the MET of the same MN with homogeneous membrane (B) drawn to a common scale of space constants. Both METs show attenuations of somatopetal PSP propagation (‘Vin mode’ in NEURON) at DC input (frequency = 0 Hz), recording electrode was at mid-soma, stimulating electrode was at mid-points of dendritic compartments. Dendritic and somatic specific membrane resistances (Rmd and Rms) were equally 8348 Ωcm2 for the homogeneous soma-dendritic membrane, while for the MET with inhomogeneous membrane Rmd and Rms were 20000 and 1046 Ωcm2 respectively. With these Rms and Rmd values the somatic input resistance was 5 MΩ in both membrane models of the MN.

Mentions: Since it is difficult to infer how MNs’ dendritic architecture affects electrical signal propagation, we used the graphical approach of the morphoelectrotonic transformation (MET, [35]). By this method it was possible to analyze the somatopetally propagating PSPs and to relate their rates of attenuations to the geometry of dendrites. We illustrated this relationship in Figure 6, where part A shows the geometrical structure of an individual cervical motoneuron (C-167), while parts B-C show two METs of the same MN. The MET maps the anatomical architecture of the dendrites to electrotonic space using the log attenuation of PSPs as the distance metric keeping the original topology and branching angles allowing visual comparison of morphology and signal propagation in dendrites. Comparisons are easy because the distances in the METs are proportional to the logarithm of the ratio of time integrals of the voltage responses at any two points, the metric used to measure attenuations of PSPs [35]. Beside the dendritic geometry, the MET is also dependent on the biophysical properties of neurons. Therefore, four METs were created for each cervical and lumbar MN. We studied the METs of MNs with physiologically constrained homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (see Methods) at different neuron resistances.


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)

Dendritic morphology and morphoelectrotonic transforms of a cervical motoneuron. Morphology (A) and METs (B) and (C) of the same MN (C-167) with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendrite membranes constrained by the physiological 5 MΩ somatic input resistance of the MN for both METs. Arrows 1 and 2 point to homologous proximal (red) and distal (green) dendritic branches where changes during METs are visibly non-proportional to their geometrical sizes (for quantitative analysis see body text). Arrows labeled by S point to the center of the soma (its entire shape is not shown in the figures). D-dorsal, V-ventral, M-medial, L-lateral directions. Note the different size of the MET with our choice of the physiologically constrained pair of Rms-Rmd values in the inhomogeneous soma-dendritic membrane (C) relative to the MET of the same MN with homogeneous membrane (B) drawn to a common scale of space constants. Both METs show attenuations of somatopetal PSP propagation (‘Vin mode’ in NEURON) at DC input (frequency = 0 Hz), recording electrode was at mid-soma, stimulating electrode was at mid-points of dendritic compartments. Dendritic and somatic specific membrane resistances (Rmd and Rms) were equally 8348 Ωcm2 for the homogeneous soma-dendritic membrane, while for the MET with inhomogeneous membrane Rmd and Rms were 20000 and 1046 Ωcm2 respectively. With these Rms and Rmd values the somatic input resistance was 5 MΩ in both membrane models of the MN.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Dendritic morphology and morphoelectrotonic transforms of a cervical motoneuron. Morphology (A) and METs (B) and (C) of the same MN (C-167) with homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendrite membranes constrained by the physiological 5 MΩ somatic input resistance of the MN for both METs. Arrows 1 and 2 point to homologous proximal (red) and distal (green) dendritic branches where changes during METs are visibly non-proportional to their geometrical sizes (for quantitative analysis see body text). Arrows labeled by S point to the center of the soma (its entire shape is not shown in the figures). D-dorsal, V-ventral, M-medial, L-lateral directions. Note the different size of the MET with our choice of the physiologically constrained pair of Rms-Rmd values in the inhomogeneous soma-dendritic membrane (C) relative to the MET of the same MN with homogeneous membrane (B) drawn to a common scale of space constants. Both METs show attenuations of somatopetal PSP propagation (‘Vin mode’ in NEURON) at DC input (frequency = 0 Hz), recording electrode was at mid-soma, stimulating electrode was at mid-points of dendritic compartments. Dendritic and somatic specific membrane resistances (Rmd and Rms) were equally 8348 Ωcm2 for the homogeneous soma-dendritic membrane, while for the MET with inhomogeneous membrane Rmd and Rms were 20000 and 1046 Ωcm2 respectively. With these Rms and Rmd values the somatic input resistance was 5 MΩ in both membrane models of the MN.
Mentions: Since it is difficult to infer how MNs’ dendritic architecture affects electrical signal propagation, we used the graphical approach of the morphoelectrotonic transformation (MET, [35]). By this method it was possible to analyze the somatopetally propagating PSPs and to relate their rates of attenuations to the geometry of dendrites. We illustrated this relationship in Figure 6, where part A shows the geometrical structure of an individual cervical motoneuron (C-167), while parts B-C show two METs of the same MN. The MET maps the anatomical architecture of the dendrites to electrotonic space using the log attenuation of PSPs as the distance metric keeping the original topology and branching angles allowing visual comparison of morphology and signal propagation in dendrites. Comparisons are easy because the distances in the METs are proportional to the logarithm of the ratio of time integrals of the voltage responses at any two points, the metric used to measure attenuations of PSPs [35]. Beside the dendritic geometry, the MET is also dependent on the biophysical properties of neurons. Therefore, four METs were created for each cervical and lumbar MN. We studied the METs of MNs with physiologically constrained homogeneous (Rms = Rmd) and inhomogeneous (Rms < Rmd) soma-dendritic membranes (see Methods) at different neuron resistances.

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