Decreased monosynaptic sensory input to an identified motoneuron is associated with steroid-mediated dendritic regression during metamorphosis in Manduca sexta

Abstract

The proleg withdrawal reflex of Manduca sexta larvae is mediated by mono- and polysynaptic connections from afferents innervating mechanosensory planta hairs (PHs) to ipsilateral proleg retractor motoneurons. During the larval-pupal transformation, a rise in ecdysteroids causes the dendrites of proleg motoneurons to regress and, concurrently, the proleg withdrawal reflex is lost. The objective of this study was to identify synaptic correlates of dendritic regression that contributed to this behavioral change. The accessory planta retractor (APR) motoneuron regresses during the larval- pupal transformation and dies in a segment-specific pattern after pupation. The compound excitatory postsynaptic potential (cEPSP) evoked in APR by electrically stimulating the proleg sensory nerve decreased in amplitude during the larval-pupal transformation. The developmental decrease in cEPSP amplitude, the extent of APR's regression, and several of APR's intrinsic electrical properties were similar in segments in which the motoneuron was fated to live or die. In heterochronic mosaic pupae bearing retained larval PH afferents, APR's dendritic regression was associated with decreases in both the mean-amplitude of monosynaptic EPSPs produced by PH afferents and the proportion of PH afferents that produced detectable EPSPs. These changes appeared due to a developmental decrease in the size of the synaptic currents produced by PH afferents. Evidence was also obtained suggesting that PH afferents do not regress at pupation. These findings support the hypothesis that the ecdysteroid-mediated regression of proleg motoneuron dendrites disconnects them from sensory inputs and, thereby, contributes to the elimination of the proleg withdrawal reflex.