Journal of Neuroscience, Vol 9, 1045-1054, Copyright © 1989 by Society for Neuroscience
Expansion of the central arborizations of persistent sensory neurons during insect metamorphosis: the role of the steroid hormone, 20- hydroxyecdysone
RB Levine
Arizona Research Laboratories Division of Neurobiology, University of Arizona, Tucson 85721.
During insect metamorphosis many larval neurons persist but are modified to
serve new behavioral roles at later stages of life. For example, certain
larval mechanosensory neurons expand their central arborizations during
pupal development and evoke a different behavioral response, the gin trap
reflex. The role of the insect steroid hormone, 20-hydroxyecdysone (20-HE)
in this developmental change was investigated by removing the normal source
of the hormone, followed by topical application of 20-HE to the peripheral
somata of the sensory neurons. In prepupal animals that were ligated
between the abdomen and thorax to remove the source of ecdysteroids the
sensory neurons retained a larval arborization pattern. Topical application
of 20-HE to the peripheral sensory neuron somata caused the treated neurons
to undergo terminal arbor expansion within the CNS. The treated sensory
neurons were not able to evoke the normal pupal behavioral response, but
instead caused a larval-like reflex response. In a previous study, sensory
neurons that were treated peripherally with a juvenile hormone analog
during the commitment peak of ecdysteroids were shown to retain a larval
arborization pattern at pupation and to not evoke the gin trap reflex
(Levine et al., 1986). Within 4 d of pupation, however, these neurons
belatedly developed expanded terminal arbors and evoked the pupal reflex.
In the present study, similarly treated animals were ligated at pupation to
block the surge in ecdysteroids that normally occurs at this time. This
treatment prevented both the delayed expansion and the reflex, whereas
topical 20-HE application induced growth and allowed the treated sensory
neurons to evoke the gin trap reflex. It is concluded that both 20-HE and
juvenile hormone act directly on the cell bodies of the sensory neurons to
regulate the growth of their central processes. This growth is necessary
but not sufficient for the development of the gin trap reflex, suggesting
that other steroid-dependent changes must also occur within the CNS. Thus,
as in the vertebrates, steroid hormones direct important developmental
events within the insect nervous system.