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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

AN dendrites and N5 axons reorganized their neuronal structure to grow toward one another after deafferentation in adult crickets. N5 (red) is composed in part of axons that carry auditory information from the tympanal organ on the cricket's forelegs to the prothoracic ganglion where a variety of neurons, including AN-2 (green), receive the auditory information and send this information to the brain. (A) The schematic of a prothoracic ganglion in a control animal shows that AN-2 as well as N5 are bilaterally symmetric. The N5 axonal terminal structure resembles a “claw” shape. AN-2 dendrites are arranged in an L shape, with medial dendrites (M) synapsing with the upper portion of the ipsilateral N5 claw and lateral dendrites (L) extending into the N5 axonal track. Postsynaptic information is relayed to the brain via the AN-2 axon (Ax) that extends through the anterior end of the prothoracic ganglion. The AN-2 soma (S) is located on the contralateral side of the midline from its dendrites. In control animals a few N5 axons may extend across the midline (arrowheads) while AN-2 dendrites tend to respect the midline. (B) After one foreleg is removed (X) in an adult cricket, deafferented AN medial dendrites grow across the midline toward the contralateral N5. In addition, N5 axons on the intact side extend toward the deafferented AN dendrites. Only a small portion of total post-deafferentation N5 growth crosses the midline (arrows indicate the area where the majority of N5 compensatory growth emerges). 40× z-stack confocal images of (C) control, (D) 3 days, (E) 7 days, and (F) 14 days deafferents display general AN and N5 anatomy and increasing amounts of growth following deafferentation. In order to see clearly the dendrites at the midline, a subset of this cell's optical sections were projected. The lateral dendrites of this cell were in optical sections that were not included in this projection. The dotted lines represent approximated midlines. Scale bars = 20 μm.
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Figure 1: AN dendrites and N5 axons reorganized their neuronal structure to grow toward one another after deafferentation in adult crickets. N5 (red) is composed in part of axons that carry auditory information from the tympanal organ on the cricket's forelegs to the prothoracic ganglion where a variety of neurons, including AN-2 (green), receive the auditory information and send this information to the brain. (A) The schematic of a prothoracic ganglion in a control animal shows that AN-2 as well as N5 are bilaterally symmetric. The N5 axonal terminal structure resembles a “claw” shape. AN-2 dendrites are arranged in an L shape, with medial dendrites (M) synapsing with the upper portion of the ipsilateral N5 claw and lateral dendrites (L) extending into the N5 axonal track. Postsynaptic information is relayed to the brain via the AN-2 axon (Ax) that extends through the anterior end of the prothoracic ganglion. The AN-2 soma (S) is located on the contralateral side of the midline from its dendrites. In control animals a few N5 axons may extend across the midline (arrowheads) while AN-2 dendrites tend to respect the midline. (B) After one foreleg is removed (X) in an adult cricket, deafferented AN medial dendrites grow across the midline toward the contralateral N5. In addition, N5 axons on the intact side extend toward the deafferented AN dendrites. Only a small portion of total post-deafferentation N5 growth crosses the midline (arrows indicate the area where the majority of N5 compensatory growth emerges). 40× z-stack confocal images of (C) control, (D) 3 days, (E) 7 days, and (F) 14 days deafferents display general AN and N5 anatomy and increasing amounts of growth following deafferentation. In order to see clearly the dendrites at the midline, a subset of this cell's optical sections were projected. The lateral dendrites of this cell were in optical sections that were not included in this projection. The dotted lines represent approximated midlines. Scale bars = 20 μm.

Mentions: Backfills using neuronal tracers allowed us to visualize AN dendrites (for simplicity, only AN-2 is shown in green) and N5 axons (red) in the same prothoracic ganglia in control adult crickets (Figure 1). Our backfills typically result in robust fills of AN-2, but sometimes include weak or incomplete backfills of AN-1 as well. Given the close proximity and overlap of AN-1 and AN-2 dendrites, we will refer to these dendrites more generally as “AN” dendrites throughout. As has been established for this system (Hoy et al., 1985; Schmitz, 1989; Horch et al., 2011), the AN dendrites from a single cell remain largely on one side of the ganglion and do not cross the mid-line in significant numbers. The majority of N5 axons also roughly respect the midline, though as has been previously noted (Schmitz, 1989), several axons extend across the midline in many normal control animals (Figures 1A,C, arrowheads). Our double backfills confirm this anatomical arrangement in the prothoracic ganglia of adult control crickets (Figure 1C).


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)

AN dendrites and N5 axons reorganized their neuronal structure to grow toward one another after deafferentation in adult crickets. N5 (red) is composed in part of axons that carry auditory information from the tympanal organ on the cricket's forelegs to the prothoracic ganglion where a variety of neurons, including AN-2 (green), receive the auditory information and send this information to the brain. (A) The schematic of a prothoracic ganglion in a control animal shows that AN-2 as well as N5 are bilaterally symmetric. The N5 axonal terminal structure resembles a “claw” shape. AN-2 dendrites are arranged in an L shape, with medial dendrites (M) synapsing with the upper portion of the ipsilateral N5 claw and lateral dendrites (L) extending into the N5 axonal track. Postsynaptic information is relayed to the brain via the AN-2 axon (Ax) that extends through the anterior end of the prothoracic ganglion. The AN-2 soma (S) is located on the contralateral side of the midline from its dendrites. In control animals a few N5 axons may extend across the midline (arrowheads) while AN-2 dendrites tend to respect the midline. (B) After one foreleg is removed (X) in an adult cricket, deafferented AN medial dendrites grow across the midline toward the contralateral N5. In addition, N5 axons on the intact side extend toward the deafferented AN dendrites. Only a small portion of total post-deafferentation N5 growth crosses the midline (arrows indicate the area where the majority of N5 compensatory growth emerges). 40× z-stack confocal images of (C) control, (D) 3 days, (E) 7 days, and (F) 14 days deafferents display general AN and N5 anatomy and increasing amounts of growth following deafferentation. In order to see clearly the dendrites at the midline, a subset of this cell's optical sections were projected. The lateral dendrites of this cell were in optical sections that were not included in this projection. The dotted lines represent approximated midlines. Scale bars = 20 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3750946&req=5

Figure 1: AN dendrites and N5 axons reorganized their neuronal structure to grow toward one another after deafferentation in adult crickets. N5 (red) is composed in part of axons that carry auditory information from the tympanal organ on the cricket's forelegs to the prothoracic ganglion where a variety of neurons, including AN-2 (green), receive the auditory information and send this information to the brain. (A) The schematic of a prothoracic ganglion in a control animal shows that AN-2 as well as N5 are bilaterally symmetric. The N5 axonal terminal structure resembles a “claw” shape. AN-2 dendrites are arranged in an L shape, with medial dendrites (M) synapsing with the upper portion of the ipsilateral N5 claw and lateral dendrites (L) extending into the N5 axonal track. Postsynaptic information is relayed to the brain via the AN-2 axon (Ax) that extends through the anterior end of the prothoracic ganglion. The AN-2 soma (S) is located on the contralateral side of the midline from its dendrites. In control animals a few N5 axons may extend across the midline (arrowheads) while AN-2 dendrites tend to respect the midline. (B) After one foreleg is removed (X) in an adult cricket, deafferented AN medial dendrites grow across the midline toward the contralateral N5. In addition, N5 axons on the intact side extend toward the deafferented AN dendrites. Only a small portion of total post-deafferentation N5 growth crosses the midline (arrows indicate the area where the majority of N5 compensatory growth emerges). 40× z-stack confocal images of (C) control, (D) 3 days, (E) 7 days, and (F) 14 days deafferents display general AN and N5 anatomy and increasing amounts of growth following deafferentation. In order to see clearly the dendrites at the midline, a subset of this cell's optical sections were projected. The lateral dendrites of this cell were in optical sections that were not included in this projection. The dotted lines represent approximated midlines. Scale bars = 20 μm.
Mentions: Backfills using neuronal tracers allowed us to visualize AN dendrites (for simplicity, only AN-2 is shown in green) and N5 axons (red) in the same prothoracic ganglia in control adult crickets (Figure 1). Our backfills typically result in robust fills of AN-2, but sometimes include weak or incomplete backfills of AN-1 as well. Given the close proximity and overlap of AN-1 and AN-2 dendrites, we will refer to these dendrites more generally as “AN” dendrites throughout. As has been established for this system (Hoy et al., 1985; Schmitz, 1989; Horch et al., 2011), the AN dendrites from a single cell remain largely on one side of the ganglion and do not cross the mid-line in significant numbers. The majority of N5 axons also roughly respect the midline, though as has been previously noted (Schmitz, 1989), several axons extend across the midline in many normal control animals (Figures 1A,C, arrowheads). Our double backfills confirm this anatomical arrangement in the prothoracic ganglia of adult control crickets (Figure 1C).

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