Journal of Neuroscience, Vol 10, 1341-1356, Copyright © 1990 by Society for Neuroscience
Postsynaptic changes at a sensory-to-motoneuron synapse contribute to the developmental loss of a reflex behavior during insect metamorphosis
GA Jacobs and JC Weeks
Department of Entomological Sciences, University of California, Berkeley 94720.
The larval-pupal transformation of the tobacco hornworm, Manduca sexta,
involves the loss of many larval-specific behaviors, including a simple
withdrawal reflex of the abdominal prolegs. This reflex is mediated by
monosynaptic excitatory connections between afferents that innervate
mechanosensory hairs on the proleg [the planta hairs (PHs)] and motoneurons
that innervate proleg retractor muscles. In response to hormonal cues
during the final days of larval life, the dendritic arbors of proleg
retractor motoneurons regress extensively. Intracellular recordings
indicate that the synaptic depolarization evoked in proleg motoneurons by
electrical stimulation of PH afferents decreases by 78% during the
larval-pupal transformation, over the same time course that the motoneuron
dendrites regress. During the same period the number of PH afferents and
the extent of their central projections may decrease slightly. To test the
relative contributions of developmental changes in the presynaptic
afferents and postsynaptic motoneurons to the weakening of the reflex
pathway, we generated heterochronic mosaic pupae that retained one larval
proleg. The PH afferents on the retained proleg retained their larval
characteristics while their postsynaptic targets, the proleg motoneurons,
appeared to regress normally. In the mosaic hemisegments, electrical
stimulation of PH afferents evoked only a small synaptic depolarization of
the proleg motoneurons, similar in amplitude to that recorded in normally
developing pupae; thus, the developmental status of the afferents was
irrelevant to the loss of the reflex. These findings suggest that
postsynaptic changes, e.g., structural regression of motoneuron dendrites,
may cause the weakening of the reflex pathway. This is the first
demonstrated correlation between the hormonally mediated regression of
motoneuron dendrites and the loss of a specific behavior during
metamorphosis.