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Neuron hemilineages provide the functional ground plan for the Drosophila ventral nervous system.

Harris RM, Pfeiffer BD, Rubin GM, Truman JW - Elife (2015)

Bottom Line: The next level was hemilineages of similar projection cells that drove intersegmentally coordinated behaviors such as walking.The highest level involved hemilineages whose activation elicited complex behaviors such as takeoff.These activation phenotypes indicate that the hemilineages vary in their behavioral roles with some contributing to local networks for sensorimotor processing and others having higher order functions of coordinating these local networks into complex behavior.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
Drosophila central neurons arise from neuroblasts that generate neurons in a pair-wise fashion, with the two daughters providing the basis for distinct A and B hemilineage groups. 33 postembryonically-born hemilineages contribute over 90% of the neurons in each thoracic hemisegment. We devised genetic approaches to define the anatomy of most of these hemilineages and to assessed their functional roles using the heat-sensitive channel dTRPA1. The simplest hemilineages contained local interneurons and their activation caused tonic or phasic leg movements lacking interlimb coordination. The next level was hemilineages of similar projection cells that drove intersegmentally coordinated behaviors such as walking. The highest level involved hemilineages whose activation elicited complex behaviors such as takeoff. These activation phenotypes indicate that the hemilineages vary in their behavioral roles with some contributing to local networks for sensorimotor processing and others having higher order functions of coordinating these local networks into complex behavior.

No MeSH data available.


Related in: MedlinePlus

Relationship of hemilineages to neuron type and to classes of evoked behavior.(A) Summary of the range of behaviors in decapitated flies elicited by stimulation of the neurons in each of the hemilineage groups using TRPA1 expression and a heat ramp to activate the temperature-sensitive channel. Behaviors are divided into six categories explained in the text. Hemilineages are arranged according to the complexity of their behavioral responses. Most behavioral responses were sustained but a few hemilineages (*) showed a progression of behaviors during the heat ramp. Diagrams show the extent of the hemilineage's arbor in transverse views of the ventral nervous system at the level of the mesothorax (T2). The numbers of flies analyzed in each group ranged from 15 to 25. (B) Registration of the hemilineage arbors to a common outline and then overlapping the hemilineage groups in which at least 50% of the individuals showed the indicated types of behavior.DOI:http://dx.doi.org/10.7554/eLife.04493.038
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fig9: Relationship of hemilineages to neuron type and to classes of evoked behavior.(A) Summary of the range of behaviors in decapitated flies elicited by stimulation of the neurons in each of the hemilineage groups using TRPA1 expression and a heat ramp to activate the temperature-sensitive channel. Behaviors are divided into six categories explained in the text. Hemilineages are arranged according to the complexity of their behavioral responses. Most behavioral responses were sustained but a few hemilineages (*) showed a progression of behaviors during the heat ramp. Diagrams show the extent of the hemilineage's arbor in transverse views of the ventral nervous system at the level of the mesothorax (T2). The numbers of flies analyzed in each group ranged from 15 to 25. (B) Registration of the hemilineage arbors to a common outline and then overlapping the hemilineage groups in which at least 50% of the individuals showed the indicated types of behavior.DOI:http://dx.doi.org/10.7554/eLife.04493.038

Mentions: A number of observations come from the analysis of the responses to the activation of the different hemilineage groups (Figure 9). The response to the stimulation of the interneuron group was quite stereotyped and highly reproducible for only a few of the hemilineages. This response consistency was confined to some of the hemilineage groups that evoked postural changes. We do not have detailed transmitter information for all of the hemilineage groups but we do know that the 9A and 5B clusters are GABA-immunopositive neurons (Harris, 2012). Therefore, the stereotypy resulting from their activation may be due to imposing inhibition at a particular level of sensory-motor integration. The hemilineages that evoked more complex behaviors typically showed a range of behaviors, although there was usually a dominant category of response that characterized that particular hemilineage group. Therefore, for these more complex behaviors, the response to hemilineage group stimulation was probabilistic rather than deterministic, in that the activity of these neurons enhanced the probability that a particular behavior would be performed. A similar phenomenon was seen in the behavioral responses of larval Drosophila to TRPA1 activation of different sparse sets of central neurons (Vogelstein et al., 2014). The larval behavioral responses also tended to be probabilistic in that a given set of neurons enhanced the probability of a behavioral response but their activity did not invariably lead to this response. Our discussion below focuses on the most frequently shown behaviors seen during the stimulation of each neuronal group.10.7554/eLife.04493.038Figure 9.Relationship of hemilineages to neuron type and to classes of evoked behavior.


Neuron hemilineages provide the functional ground plan for the Drosophila ventral nervous system.

Harris RM, Pfeiffer BD, Rubin GM, Truman JW - Elife (2015)

Relationship of hemilineages to neuron type and to classes of evoked behavior.(A) Summary of the range of behaviors in decapitated flies elicited by stimulation of the neurons in each of the hemilineage groups using TRPA1 expression and a heat ramp to activate the temperature-sensitive channel. Behaviors are divided into six categories explained in the text. Hemilineages are arranged according to the complexity of their behavioral responses. Most behavioral responses were sustained but a few hemilineages (*) showed a progression of behaviors during the heat ramp. Diagrams show the extent of the hemilineage's arbor in transverse views of the ventral nervous system at the level of the mesothorax (T2). The numbers of flies analyzed in each group ranged from 15 to 25. (B) Registration of the hemilineage arbors to a common outline and then overlapping the hemilineage groups in which at least 50% of the individuals showed the indicated types of behavior.DOI:http://dx.doi.org/10.7554/eLife.04493.038
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4525104&req=5

fig9: Relationship of hemilineages to neuron type and to classes of evoked behavior.(A) Summary of the range of behaviors in decapitated flies elicited by stimulation of the neurons in each of the hemilineage groups using TRPA1 expression and a heat ramp to activate the temperature-sensitive channel. Behaviors are divided into six categories explained in the text. Hemilineages are arranged according to the complexity of their behavioral responses. Most behavioral responses were sustained but a few hemilineages (*) showed a progression of behaviors during the heat ramp. Diagrams show the extent of the hemilineage's arbor in transverse views of the ventral nervous system at the level of the mesothorax (T2). The numbers of flies analyzed in each group ranged from 15 to 25. (B) Registration of the hemilineage arbors to a common outline and then overlapping the hemilineage groups in which at least 50% of the individuals showed the indicated types of behavior.DOI:http://dx.doi.org/10.7554/eLife.04493.038
Mentions: A number of observations come from the analysis of the responses to the activation of the different hemilineage groups (Figure 9). The response to the stimulation of the interneuron group was quite stereotyped and highly reproducible for only a few of the hemilineages. This response consistency was confined to some of the hemilineage groups that evoked postural changes. We do not have detailed transmitter information for all of the hemilineage groups but we do know that the 9A and 5B clusters are GABA-immunopositive neurons (Harris, 2012). Therefore, the stereotypy resulting from their activation may be due to imposing inhibition at a particular level of sensory-motor integration. The hemilineages that evoked more complex behaviors typically showed a range of behaviors, although there was usually a dominant category of response that characterized that particular hemilineage group. Therefore, for these more complex behaviors, the response to hemilineage group stimulation was probabilistic rather than deterministic, in that the activity of these neurons enhanced the probability that a particular behavior would be performed. A similar phenomenon was seen in the behavioral responses of larval Drosophila to TRPA1 activation of different sparse sets of central neurons (Vogelstein et al., 2014). The larval behavioral responses also tended to be probabilistic in that a given set of neurons enhanced the probability of a behavioral response but their activity did not invariably lead to this response. Our discussion below focuses on the most frequently shown behaviors seen during the stimulation of each neuronal group.10.7554/eLife.04493.038Figure 9.Relationship of hemilineages to neuron type and to classes of evoked behavior.

Bottom Line: The next level was hemilineages of similar projection cells that drove intersegmentally coordinated behaviors such as walking.The highest level involved hemilineages whose activation elicited complex behaviors such as takeoff.These activation phenotypes indicate that the hemilineages vary in their behavioral roles with some contributing to local networks for sensorimotor processing and others having higher order functions of coordinating these local networks into complex behavior.

View Article: PubMed Central - PubMed

Affiliation: Janelia Research Campus, Howard Hughes Medical Institute, Ashburn, United States.

ABSTRACT
Drosophila central neurons arise from neuroblasts that generate neurons in a pair-wise fashion, with the two daughters providing the basis for distinct A and B hemilineage groups. 33 postembryonically-born hemilineages contribute over 90% of the neurons in each thoracic hemisegment. We devised genetic approaches to define the anatomy of most of these hemilineages and to assessed their functional roles using the heat-sensitive channel dTRPA1. The simplest hemilineages contained local interneurons and their activation caused tonic or phasic leg movements lacking interlimb coordination. The next level was hemilineages of similar projection cells that drove intersegmentally coordinated behaviors such as walking. The highest level involved hemilineages whose activation elicited complex behaviors such as takeoff. These activation phenotypes indicate that the hemilineages vary in their behavioral roles with some contributing to local networks for sensorimotor processing and others having higher order functions of coordinating these local networks into complex behavior.

No MeSH data available.


Related in: MedlinePlus