Habituation of the proleg withdrawal reflex in Manduca sexta does not involve changes in motoneuron properties or depression at the sensorimotor synapse.

Larvae of the hawkmoth, Manduca sexta, exhibit a defensive proleg withdrawal reflex in which deflection of mechanosensory hairs on the proleg tip (the planta) evokes retraction of the proleg. A previous behavioral study showed that this reflex habituates in response to repeated planta hair deflection and exhibits several other defining features of habituation. In a semi-intact preparation consisting of a proleg and its associated segmental ganglion, repeated deflection of a planta hair or electrical stimulation of its sensory neuron causes a neural correlate of habituation, manifested as a decrease in the number of action potentials evoked in the proleg motor nerve. Monosynaptic connections from planta hair sensory neurons to the principal planta retractor motoneuron exhibit several forms of activity-dependent plasticity. In the present study we recorded intracellularly from this motoneuron during repetitive electrical stimulation of a planta hair sensory neuron. The number of action potentials evoked in the motoneuron decreased significantly, representing a neural correlate of habituation. The motoneuron's resting membrane potential, input resistance. and spike threshold measured before and after repetitive stimulation did not differ between the stimulated group and a control group. Furthermore, the amplitude of the monosynaptic excitatory postsynaptic potential, as well as the magnitude of paired-pulse facilitation, evoked in the motoneuron by the sensory neuron did not change after repetitive stimulation. These results suggest that depression at the sensorimotor synapse does not contribute to reflex habituation. Rather, other mechanisms in the ganglion of the stimulated segment, such as changes in polysynaptic reflex pathways, appear to be responsible.

Neural correlates of habituation of the proleg withdrawal reflex in larvae of the hawk moth, Manduca sexta.

The larval proleg withdrawal reflex of the hawk moth, Manduca sexta, exhibits robust habituation. This reflex is evoked by deflecting one or more mechanosensory planta hairs on a proleg tip. We examined neural correlates of habituation in an isolated proleg preparation consisting of one proleg and its segmental ganglion. Repeated deflection of a single planta hair caused a significant decrease in the number of action potentials evoked in the proleg motor nerve (which carries the axons of proleg retractor motor neurons). Significant response decrement was seen for interstimulus intervals of 10 s, 60 s and 5 min. Response decrement failed to occur in the absence of repetitive stimulation, the decremented response recovered spontaneously following a rest, and electrical stimulation of a body wall nerve facilitated the decremented response (a neural correlate of dishabituation). Adaptation of sensory neuron responses occurred during repeated hair deflections. However, when adaptation was eliminated by direct electrical stimulation of sensory neurons, the response in the proleg motor nerve still decreased significantly. Muscle recordings indicated that the response of an identified proleg retractor motor neuron decreased significantly during habituation training. Thus, habituation of the proleg withdrawal reflex includes a central component that is apparent at the level of a single motor neuron.

Neural mechanisms of behavioral plasticity: metamorphosis and learning in Manduca sexta.

This review summarizes our current understanding of the neural circuit underlying the larval proleg withdrawal reflex (PWR) of Manduca sexta and describes how PWR function changes in two contexts: metamorphosis and learning. The first form of PWR plasticity occurs during the larval-pupal transformation, when the reflex is lost. One mechanism that contributes to this loss is the weakening of monosynaptic excitatory connection from proleg sensory neurons to proleg retractor motor neurons. This change is associated with the hormonally-mediated regression of proleg motor neuron dendrites, which may break synaptic contacts between the sensory and motor neurons. After pupation, some of the proleg motor neurons die in a segment-specific pattern that persists even after individual motor neurons are isolated from the nervous system and exposed to hormones in vitro. The second form of PWR plasticity involves short-term, activity-dependent changes in neural function during the larval stage. The nicotinic cholinergic connections from proleg sensory neurons to motor neurons exhibit several forms of plasticity including facilitation, depression, post-tetanic potentiation and two types of muscarinic modulation. Larval PWR behavior exhibits two simple forms of learning-habituation and dishabituation-which involve alterations in the central PWR circuit. These studies of a simple circuit illustrate neural mechanisms by which behaviors undergo both short- and long-term modifications.

Habituation and dishabituation of the proleg withdrawal reflex in larvae of the sphinx hawk, Manduca sexta.

The neural circuit for the proleg withdrawal reflex (PWR) of Manduca sexta larvae exhibits activity-dependent plasticity. This study demonstrates habituation and dishabituation of PWR behavior. Repeated deflection of 1 or 5 mechanosensory hairs on a proleg at a 60-s interstimulus interval (ISI) for 20 trials produced a significant decrease in evoked force of proleg withdrawal. Habituation was similar with 30-s and 60-s ISIs and nonsignificant with a 5-min ISI or without repeated stimulation. Habituated responses recovered after cessation of stimulation or pinch of the body wall (dishabituation). The role of intersegmental influences was tested by severing connectives to leave different numbers of ganglia connected to the test segment. Habituation was robust even in test segments that were disconnected from the rest of the central nervous system. The PWR of Manduca is appropriate for further analysis of cellular mechanisms underlying learning.