Steroid-Induced Dendritic Regression Reduces Anatomical Contacts between Neurons during Synaptic Weakening and the Developmental Loss of a Behavior

Steroid hormones alter dendritic architecture in many animals, but the exact relationship between dendritic anatomy, synaptic strength, and behavioral expression is typically unknown. In larvae of the mothManduca sexta, the tip of each abdominal proleg (locomotory appendage) bears an array of mechanosensory hairs, each innervated by a planta hair sensory neuron (PH-SN). In the CNS, PH-SN axons make monosynaptic, excitatory nicotinic cholinergic connections with accessory planta retractor (APR) motoneurons. These synapses mediate a proleg withdrawal reflex behavior that is lost at pupation. The prepupal peak of ecdysteroids (molting hormones) triggers the regression of APR dendrites and a >80% reduction in the amplitude of EPSPs produced in APRs by PH-SNs that innervate posterior planta hairs. The present study tested the hypothesis that a decrease in the number of synaptic contacts from PH-SNs to APRs contributes to this synaptic weakening. Pairs of PH-SNs and APRs were fluorescently labeled in larvae and pupae, and the number of indistinguishably close anatomical contacts (putative synapses) was counted by confocal laser scanning microscopy. During APR dendritic regression, the mean number of contacts from posterior PH-SNs decreased by ∼80%, whereas the size of individual contacts did not change detectably and the axonal arbors of PH-SNs did not regress. These results suggest that the steroid-induced regression of motoneuron dendrites physically disconnects the motoneurons from the synaptic terminals of sensory neurons, producing synaptic weakening and the developmental loss of the proleg withdrawal reflex behavior at pupation.