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Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus.

Pfister A, Johnson A, Ellers O, Horch HW - Front Physiol (2013)

Bottom Line: However, the cues that maintain or influence adult neuronal morphology are less well understood.In males, however, dendritic growth rates were linear, with dendrites growing steadily over time and reaching lengths, on average, twice as long as in females.On the other hand, rates of N5 axonal growth showed no significant sexual dimorphism and were linear.

View Article: PubMed Central - PubMed

Affiliation: Department of Invertebrate Zoology, American Museum of Natural History New York, NY, USA.

ABSTRACT
Dendrite and axon growth and branching during development are regulated by a complex set of intracellular and external signals. However, the cues that maintain or influence adult neuronal morphology are less well understood. Injury and deafferentation tend to have negative effects on adult nervous systems. An interesting example of injury-induced compensatory growth is seen in the cricket, Gryllus bimaculatus. After unilateral loss of an ear in the adult cricket, auditory neurons within the central nervous system (CNS) sprout to compensate for the injury. Specifically, after being deafferented, ascending neurons (AN-1 and AN-2) send dendrites across the midline of the prothoracic ganglion where they receive input from auditory afferents that project through the contralateral auditory nerve (N5). Deafferentation also triggers contralateral N5 axonal growth. In this study, we quantified AN dendritic and N5 axonal growth at 30 h, as well as at 3, 5, 7, 14, and 20 days after deafferentation in adult crickets. Significant differences in the rates of dendritic growth between males and females were noted. In females, dendritic growth rates were non-linear; a rapid burst of dendritic extension in the first few days was followed by a plateau reached at 3 days after deafferentation. In males, however, dendritic growth rates were linear, with dendrites growing steadily over time and reaching lengths, on average, twice as long as in females. On the other hand, rates of N5 axonal growth showed no significant sexual dimorphism and were linear. Within each animal, the growth rates of dendrites and axons were not correlated, indicating that independent factors likely influence dendritic and axonal growth in response to injury in this system. Our findings provide a basis for future study of the cellular features that allow differing dendrite and axon growth patterns as well as sexually dimorphic dendritic growth in response to deafferentation.

No MeSH data available.


Related in: MedlinePlus

N5 extraneuropillar growth increased in the same linear pattern for males and females following deafferentation. (A) Total N5 growth consisted of the axons crossing the midline (dotted line) as well as the axons crossing the bottom edge of the anterior portion of the claw (solid white line) to extend outside of the neuropil (arrow). The volume of this extraneuropillar growth was measured. The N5 image shown belongs to a 7 days deafferent. Scale bar = 20 μm. (B) Male (blue) and female (red) N5 extraneuropillar growth data sets increased linearly and were not significantly different from one another. Black data points represent means, and error bars represent standard error of the mean. Female N5 extraneuropillar growth control (n = 7), 30 h (n = 6), 3 days (n = 5), 5 days (n = 10), 7 days (n = 6), 14 days (n = 2), and 20 days (n = 10). Male N5 extraneuropillar growth control (n = 9), 30 h (n = 6), 3 days (n = 3), 5 days (n = 7), 7 days (n = 6), 14 days (n = 7), and 20 days (n = 7). The shaded gray area represents the 95% confidence interval. See Table 2 for regression equations and statistics.
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Figure 5: N5 extraneuropillar growth increased in the same linear pattern for males and females following deafferentation. (A) Total N5 growth consisted of the axons crossing the midline (dotted line) as well as the axons crossing the bottom edge of the anterior portion of the claw (solid white line) to extend outside of the neuropil (arrow). The volume of this extraneuropillar growth was measured. The N5 image shown belongs to a 7 days deafferent. Scale bar = 20 μm. (B) Male (blue) and female (red) N5 extraneuropillar growth data sets increased linearly and were not significantly different from one another. Black data points represent means, and error bars represent standard error of the mean. Female N5 extraneuropillar growth control (n = 7), 30 h (n = 6), 3 days (n = 5), 5 days (n = 10), 7 days (n = 6), 14 days (n = 2), and 20 days (n = 10). Male N5 extraneuropillar growth control (n = 9), 30 h (n = 6), 3 days (n = 3), 5 days (n = 7), 7 days (n = 6), 14 days (n = 7), and 20 days (n = 7). The shaded gray area represents the 95% confidence interval. See Table 2 for regression equations and statistics.

Mentions: Using Volocity to scroll through sequential planes, axonal and dendritic branches were traced by hand in three dimensions. AN and N5 processes were quantified by the perpendicular extent of the point furthest from the midline (perpendicular extent), by the longest dendrite, and by skeletal length (the summed length of all the processes; Figure 2D). The volume of axons that project outside the typical medial ventral association center (mVAC) region was also measured. The upper region of the N5 “claw-shaped” arborization has a distinct posterior edge in control crickets that was approximated by a straight line for analysis. The volume of axons that projected across this line or across the mid-line was measured using Volocity (Figure 5).


Quantification of dendritic and axonal growth after injury to the auditory system of the adult cricket Gryllus bimaculatus.

Pfister A, Johnson A, Ellers O, Horch HW - Front Physiol (2013)

N5 extraneuropillar growth increased in the same linear pattern for males and females following deafferentation. (A) Total N5 growth consisted of the axons crossing the midline (dotted line) as well as the axons crossing the bottom edge of the anterior portion of the claw (solid white line) to extend outside of the neuropil (arrow). The volume of this extraneuropillar growth was measured. The N5 image shown belongs to a 7 days deafferent. Scale bar = 20 μm. (B) Male (blue) and female (red) N5 extraneuropillar growth data sets increased linearly and were not significantly different from one another. Black data points represent means, and error bars represent standard error of the mean. Female N5 extraneuropillar growth control (n = 7), 30 h (n = 6), 3 days (n = 5), 5 days (n = 10), 7 days (n = 6), 14 days (n = 2), and 20 days (n = 10). Male N5 extraneuropillar growth control (n = 9), 30 h (n = 6), 3 days (n = 3), 5 days (n = 7), 7 days (n = 6), 14 days (n = 7), and 20 days (n = 7). The shaded gray area represents the 95% confidence interval. See Table 2 for regression equations and statistics.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 5: N5 extraneuropillar growth increased in the same linear pattern for males and females following deafferentation. (A) Total N5 growth consisted of the axons crossing the midline (dotted line) as well as the axons crossing the bottom edge of the anterior portion of the claw (solid white line) to extend outside of the neuropil (arrow). The volume of this extraneuropillar growth was measured. The N5 image shown belongs to a 7 days deafferent. Scale bar = 20 μm. (B) Male (blue) and female (red) N5 extraneuropillar growth data sets increased linearly and were not significantly different from one another. Black data points represent means, and error bars represent standard error of the mean. Female N5 extraneuropillar growth control (n = 7), 30 h (n = 6), 3 days (n = 5), 5 days (n = 10), 7 days (n = 6), 14 days (n = 2), and 20 days (n = 10). Male N5 extraneuropillar growth control (n = 9), 30 h (n = 6), 3 days (n = 3), 5 days (n = 7), 7 days (n = 6), 14 days (n = 7), and 20 days (n = 7). The shaded gray area represents the 95% confidence interval. See Table 2 for regression equations and statistics.
Mentions: Using Volocity to scroll through sequential planes, axonal and dendritic branches were traced by hand in three dimensions. AN and N5 processes were quantified by the perpendicular extent of the point furthest from the midline (perpendicular extent), by the longest dendrite, and by skeletal length (the summed length of all the processes; Figure 2D). The volume of axons that project outside the typical medial ventral association center (mVAC) region was also measured. The upper region of the N5 “claw-shaped” arborization has a distinct posterior edge in control crickets that was approximated by a straight line for analysis. The volume of axons that projected across this line or across the mid-line was measured using Volocity (Figure 5).

Bottom Line: However, the cues that maintain or influence adult neuronal morphology are less well understood.In males, however, dendritic growth rates were linear, with dendrites growing steadily over time and reaching lengths, on average, twice as long as in females.On the other hand, rates of N5 axonal growth showed no significant sexual dimorphism and were linear.

View Article: PubMed Central - PubMed

Affiliation: Department of Invertebrate Zoology, American Museum of Natural History New York, NY, USA.

ABSTRACT
Dendrite and axon growth and branching during development are regulated by a complex set of intracellular and external signals. However, the cues that maintain or influence adult neuronal morphology are less well understood. Injury and deafferentation tend to have negative effects on adult nervous systems. An interesting example of injury-induced compensatory growth is seen in the cricket, Gryllus bimaculatus. After unilateral loss of an ear in the adult cricket, auditory neurons within the central nervous system (CNS) sprout to compensate for the injury. Specifically, after being deafferented, ascending neurons (AN-1 and AN-2) send dendrites across the midline of the prothoracic ganglion where they receive input from auditory afferents that project through the contralateral auditory nerve (N5). Deafferentation also triggers contralateral N5 axonal growth. In this study, we quantified AN dendritic and N5 axonal growth at 30 h, as well as at 3, 5, 7, 14, and 20 days after deafferentation in adult crickets. Significant differences in the rates of dendritic growth between males and females were noted. In females, dendritic growth rates were non-linear; a rapid burst of dendritic extension in the first few days was followed by a plateau reached at 3 days after deafferentation. In males, however, dendritic growth rates were linear, with dendrites growing steadily over time and reaching lengths, on average, twice as long as in females. On the other hand, rates of N5 axonal growth showed no significant sexual dimorphism and were linear. Within each animal, the growth rates of dendrites and axons were not correlated, indicating that independent factors likely influence dendritic and axonal growth in response to injury in this system. Our findings provide a basis for future study of the cellular features that allow differing dendrite and axon growth patterns as well as sexually dimorphic dendritic growth in response to deafferentation.

No MeSH data available.


Related in: MedlinePlus