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Persistent larval sensory neurones are required for the normal development of the adult sensory afferent projections in Drosophila

Darren W. Williams^* and David Shepherd

School of Biological Sciences, University of Southampton, Southampton, SO16 7PX, UK
^* Present address: Department of Zoology, University of Washington, Seattle, WA 98195, USA

View larger version (90K): [in a new window]   Fig. 1. Selective ablation of sensory neurones. (A-D) Dorsal is upwards and anterior towards the right. (A) Detail of the sensory neurones revealed by GAL4 line C161 driving expression of UAS-CD8GFP in a living third instar larva. Eleven sensory neurones of the dorsal and lateral clusters in the mesothorax. The two clusters are separated by the dorsal bipolar dendrite neurone (dbd). The lateral group, ventral to dbd, consists of four multidendritic neurones (ldaA, ldaB, ldaC and ldaD). The dorsal cluster, dorsal to dbd, consists of six neurones, including two chordotonal neurones (dch1 and dch2), and four multidendritic neurones (ddaA, ddaB, ddaC, ddaD). (B) Detail of the lateral cluster and dbd in a live specimen prior to laser ablation. (C) The same neurones as shown in B 12 hours after laser ablation of the four neurones ventral to dbd. One of the neurones is missing (*) and the other three neurones exhibit a condensed cell body, loss of dendrites and blebbing. (D) The same neurones 30 hours after ablation, only 2 neurones are visible and exhibit shrunken morphology and no dendritic structures. (E) Central projections of the neurones in line C161 revealed immunocytochemically with anti-GFP. The panel shows a dorsal view of the mesothoracic neuromere of the ventral nerve cord of a pupa 48 hours after unilateral laser ablation of the neurones in the dorsal and lateral cluster neurones. On the intact (right-hand) side the normal pattern of central projections is seen in which it is possible to identify three major axon pathways (med, lt and dpt). On the ablated (left-hand) side there are no central projections evident (arrow). (F) Dorsal view of the mesothoracic neuromere 48 hours after ablation of only the lateral cluster neurones. On the intact (right-hand) side the normal pattern of axons is present. On the ablated (left-hand) side only the med projection is evident. Scale bar: 50 µm.

View larger version (181K): [in a new window]   Fig. 2. The effects of laser ablation on the central projections of adult sensory neurones. Six different specimens showing the mesothoracic neuromere of the adult ventral nerve cord with sensory projections revealed immunocytochemically using GAL4 line C161 driving expression of CD8-GFP. In all panels, the ablated side is the left-hand side and anterior is upwards. (A-C) Illustrate typical defects in the central projections from the wing and notum. Typical defects include poor axon fasciculation, pathway errors and axon spiralling. (D,E) Defects in the formation of a specific terminal arborisation the posterior-dorsal projection (pd). Refer to text for detailed descriptions. Scale bar: 30 µm.

View larger version (78K): [in a new window]   Fig. 3. DiI staining of the psc neurone. (A) Central projections of the psc neurone in an untreated specimen. The neurone is formed by a single robust axon (arrowheads) entering the CNS via the dorsal wing nerve and exhibits the stereotypical features previously described for this neurone. (B) The psc neurone following unilateral ablation of the dorsal and lateral groups of sensory neurones. The neurone shows disruption to its structure at the point of entry (black arrow), as well as repeatedly crossing the midline (arrowheads) to form the posterior process (white arrows). (C) An unusual example of the psc neurone central projection following unilateral ablation of dorsal and lateral clusters. In this example, the psc has entered the CNS ectopically via the metathoracic nerve (arrows) and has formed an elaborate central projection in which elements of the normal psc projection can be recognised. Scale bar: 30 µm.

View larger version (26K): [in a new window]   Fig. 4. Detailed structure of the psc neurone in untreated and ablated specimens. (A) Five examples of the psc neurone in untreated specimens showing the consistent structure of the central projections. (B) Five examples of the psc neurone following unilateral ablation of the dorsal and lateral groups of neurones. These examples show axon splitting at the entry points as well as duplication of key structures. (C) Five examples of the psc neurone following unilateral ablation of only the dorsal groups of neurones. These examples do not show axon splitting at the entry point but all show defects associated with crossing the midline (*). (D) Five examples of the psc neurone following unilateral ablation of only the lateral groups of neurones. These examples show defects with the formation of the posterior projection. Refer to text for detailed descriptions. Lowercase lettering refers to the identity of the different sub-branches in the psc neurone.