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Dendritic orientation and branching distinguish a class of multifunctional turtle spinal interneurons.

Holmes JR, Berkowitz A - Front Neural Circuits (2014)

Bottom Line: These synaptic inputs can occur on distal dendrites and yet must remain effective at the soma.Here, we quantitatively investigated additional dendritic morphological characteristics of T neurons as compared to non-T neurons.We found that T neurons have less total dendritic length, a greater proportion of dendritic length in primary dendrites, and dendrites that are oriented more mediolaterally.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Oklahoma Norman, OK, USA.

ABSTRACT
Spinal interneurons can integrate diverse propriospinal and supraspinal inputs that trigger or modulate locomotion and other limb movements. These synaptic inputs can occur on distal dendrites and yet must remain effective at the soma. Active dendritic conductances may amplify distal dendritic inputs, but appear to play a minimal role during scratching, at least. Another possibility is that spinal interneurons that integrate inputs on distal dendrites have unusually simple dendritic trees that effectively funnel current to the soma. We previously described a class of spinal interneurons, called transverse interneurons (or T neurons), in adult turtles. T neurons were defined as having dendrites that extend further in the transverse plane than rostrocaudally and a soma that extends further mediolaterally than rostrocaudally. T neurons are multifunctional, as they were activated during both swimming and scratching motor patterns. T neurons had higher peak firing rates and larger membrane potential oscillations during scratching than scratch-activated interneurons with different dendritic morphologies ("non-T" neurons). These characteristics make T neurons good candidates to play an important role in integrating diverse inputs and generating or relaying rhythmic motor patterns. Here, we quantitatively investigated additional dendritic morphological characteristics of T neurons as compared to non-T neurons. We found that T neurons have less total dendritic length, a greater proportion of dendritic length in primary dendrites, and dendrites that are oriented more mediolaterally. Thus, T neuron dendritic trees extend far mediolaterally, yet are unusually simple, which may help channel synaptic current from distal dendrites in the lateral and ventral funiculi to the soma. In combination with T neuron physiological properties, these dendritic properties may help integrate supraspinal and propriospinal inputs and generate and/or modulate rhythmic limb movements.

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Comparisons of dendritic parameters between T neurons (n = 17) and non-T neurons (n = 14). (A) Total dendritic length. (B) Mean dendritic angle (0° = mediolateral; 90° = rostrocaudal; in horizontal sections). (C) Percentage of dendritic length by dendrite branch order. 1°, primary; 2°, secondary, etc. Vertical lines, SD; *, statistically significant difference.
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Figure 3: Comparisons of dendritic parameters between T neurons (n = 17) and non-T neurons (n = 14). (A) Total dendritic length. (B) Mean dendritic angle (0° = mediolateral; 90° = rostrocaudal; in horizontal sections). (C) Percentage of dendritic length by dendrite branch order. 1°, primary; 2°, secondary, etc. Vertical lines, SD; *, statistically significant difference.

Mentions: To test these hypotheses quantitatively, we measured the total dendritic length, proportion of dendritic length taken by primary dendrites, secondary dendrites, etc., and mean dendritic angle (the mean of the angles of all the individual dendritic segments of a neuron, weighted by the proportional length of each dendritic segment) for all the T neurons and non-T neurons (Figure 3). T neurons had significantly less total dendritic length than non-T neurons (Figure 3A; p = 0.007). T neurons also had significantly lower [i.e., closer to mediolateral (0°), as opposed to rostrocaudal (90°)] mean dendritic angles than non-T neurons (Figure 3B; p < 0.0001). In addition, T neurons appeared to have a greater proportion of dendritic length in primary dendrites and a lesser proportion in >5th-order dendrites (Figure 3C), so we compared these values statistically. The T neuron percentage of dendritic length in primary dendrites was significantly higher (p = 0.04), but the percentage in > 5th-order dendrites was not significantly lower (p = 0.13). Note that our analyses collapsed the third dimension, dorsoventral, so it is possible that the neurons’ dendritic length along the dorsoventral axis differed between groups and that this difference would have altered the differences we observed in total dendritic length.


Dendritic orientation and branching distinguish a class of multifunctional turtle spinal interneurons.

Holmes JR, Berkowitz A - Front Neural Circuits (2014)

Comparisons of dendritic parameters between T neurons (n = 17) and non-T neurons (n = 14). (A) Total dendritic length. (B) Mean dendritic angle (0° = mediolateral; 90° = rostrocaudal; in horizontal sections). (C) Percentage of dendritic length by dendrite branch order. 1°, primary; 2°, secondary, etc. Vertical lines, SD; *, statistically significant difference.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4230039&req=5

Figure 3: Comparisons of dendritic parameters between T neurons (n = 17) and non-T neurons (n = 14). (A) Total dendritic length. (B) Mean dendritic angle (0° = mediolateral; 90° = rostrocaudal; in horizontal sections). (C) Percentage of dendritic length by dendrite branch order. 1°, primary; 2°, secondary, etc. Vertical lines, SD; *, statistically significant difference.
Mentions: To test these hypotheses quantitatively, we measured the total dendritic length, proportion of dendritic length taken by primary dendrites, secondary dendrites, etc., and mean dendritic angle (the mean of the angles of all the individual dendritic segments of a neuron, weighted by the proportional length of each dendritic segment) for all the T neurons and non-T neurons (Figure 3). T neurons had significantly less total dendritic length than non-T neurons (Figure 3A; p = 0.007). T neurons also had significantly lower [i.e., closer to mediolateral (0°), as opposed to rostrocaudal (90°)] mean dendritic angles than non-T neurons (Figure 3B; p < 0.0001). In addition, T neurons appeared to have a greater proportion of dendritic length in primary dendrites and a lesser proportion in >5th-order dendrites (Figure 3C), so we compared these values statistically. The T neuron percentage of dendritic length in primary dendrites was significantly higher (p = 0.04), but the percentage in > 5th-order dendrites was not significantly lower (p = 0.13). Note that our analyses collapsed the third dimension, dorsoventral, so it is possible that the neurons’ dendritic length along the dorsoventral axis differed between groups and that this difference would have altered the differences we observed in total dendritic length.

Bottom Line: These synaptic inputs can occur on distal dendrites and yet must remain effective at the soma.Here, we quantitatively investigated additional dendritic morphological characteristics of T neurons as compared to non-T neurons.We found that T neurons have less total dendritic length, a greater proportion of dendritic length in primary dendrites, and dendrites that are oriented more mediolaterally.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, University of Oklahoma Norman, OK, USA.

ABSTRACT
Spinal interneurons can integrate diverse propriospinal and supraspinal inputs that trigger or modulate locomotion and other limb movements. These synaptic inputs can occur on distal dendrites and yet must remain effective at the soma. Active dendritic conductances may amplify distal dendritic inputs, but appear to play a minimal role during scratching, at least. Another possibility is that spinal interneurons that integrate inputs on distal dendrites have unusually simple dendritic trees that effectively funnel current to the soma. We previously described a class of spinal interneurons, called transverse interneurons (or T neurons), in adult turtles. T neurons were defined as having dendrites that extend further in the transverse plane than rostrocaudally and a soma that extends further mediolaterally than rostrocaudally. T neurons are multifunctional, as they were activated during both swimming and scratching motor patterns. T neurons had higher peak firing rates and larger membrane potential oscillations during scratching than scratch-activated interneurons with different dendritic morphologies ("non-T" neurons). These characteristics make T neurons good candidates to play an important role in integrating diverse inputs and generating or relaying rhythmic motor patterns. Here, we quantitatively investigated additional dendritic morphological characteristics of T neurons as compared to non-T neurons. We found that T neurons have less total dendritic length, a greater proportion of dendritic length in primary dendrites, and dendrites that are oriented more mediolaterally. Thus, T neuron dendritic trees extend far mediolaterally, yet are unusually simple, which may help channel synaptic current from distal dendrites in the lateral and ventral funiculi to the soma. In combination with T neuron physiological properties, these dendritic properties may help integrate supraspinal and propriospinal inputs and generate and/or modulate rhythmic limb movements.

Show MeSH