A Pair of Identified Interneurons inAplysiathat Are Involved in Multiple Behaviors Are Necessary and Sufficient for the Arterial-Shortening Component of a Local Withdrawal Reflex

Abstract

A bilateral pair of cerebral interneurons, called CC5, contribute to the generation of a number of different behaviors involving head movements. Each cell sends its axon to the ipsilateral and contralateral pedal and pleural ganglia. A weak tactile stimulus to the head excites the ipsilateral CC5; a strong stimulus excites both the ipsilateral and contralateral cells. Firing of CC5 produces powerful shortening of the ipsilateral pedal artery (PA) by means of monosynaptic excitation of the pedal artery shortener (PAS) neuron, the single motor neuron for the artery. A weak touch to a tentacle excites the ipsilateral PAS and evokes a local withdrawal response accompanied by shortening of the ipsilateral PA. In vivo recording of the pedal artery nerve (PAn) showed that PAS was activated bilaterally during defensive head withdrawal elicited by a strong stimulus and was activated unilaterally by a weak stimulus. The responses were eliminated by cutting the ipsilateral cerebral-pleural connective (C-PLC). Electrical stimulation of the cerebral-pleural connective provided evidence that all of the excitatory input to PAS via this connective is provided by CC5. A variety of experimental results indicates that during a local withdrawal reflex of the tentacle, CC5 is necessary and sufficient for the unilateral PA-shortening component of the response and therefore functions as a command neuron for a component of the behavior. The data suggest that during defensive head withdrawal, the two CC5 neurons may act conjointly as a two-neuron command system that is necessary and sufficient for the bilateral arterial-shortening component of the behavior.

An Identified Interneuron Contributes to Aspects of Six Different Behaviors inAplysia

“…The animals and methods in these experiments were similar to those described in detail in a previous paper (Xin et al, 1996). Unless otherwise mentioned, in all experiments studying the connections between neurons, we used the isolated head ganglia preparation (buccal, cerebral, and pedal-pleural) interconnected by their connectives.…”

“…What is unclear is how the activity of multifunctional neurons is translated into behavior and whether multifunctional neurons can serve different roles for different behaviors. In a companion paper, we describe an identified interneuron, CC5, that appears to be necessary and sufficient for the arterial artery shortening component of a local withdrawal response (Xin et al, 1996) (see also Skelton and Koester, 1992). In the present paper, we describe data that indicate CC5 is engaged in multiple behaviors, all of which involve movements of the neck of the animal.…”

“…Recordings from the pedal artery nerve (PAn) showed increased firing of a unit whenever the firing rate of CC5 increased. Previous data (Xin et al, 1996) strongly suggest that the unit in the nerve reflects the firing of the pedal artery shortener motor neuron (PAS), a cell that is strongly excited by CC5. In preparations that included the buccal mass, mechanical stimulation of the buccal mass evoked several cycles of buccal mass movements, and CC5 was excited during each cycle ( Fig.…”

“…CC5 affects the activity of neurons that send axons into the pleural and pedal nerves, and the cerebralbuccal and pleural-abdominal connectives Because CC5 previously was found to receive differential sensory input from the ipsilateral and contralateral regions of the head (Xin et al, 1996), we examined the possibility that CC5 may be involved in asymmetric head movements, such as those that occur during head waving and directed head turning. Accordingly, we examined whether firing of CC5 could affect the activity of units recorded from pedal and pleural ganglion nerves that control various regions of the neck and foot.…”

“…The unit activity evoked by CC5 was consistent within a preparation, but was somewhat variable from preparation to preparation. The effect of CC5 on the CBC unit was blocked when the axon of CC5 that travels out of the cerebral ganglion to the pedal-pleural ganglion via the cerebral-pleural (C-PL) connective was interrupted by cutting the C-PL connective [for a diagram of the course of the CC5 axon into the connectives, see Xin et al (1996), their Fig. 2].…”