An Identified Interneuron Contributes to Aspects of Six Different Behaviors inAplysia

Abstract

Previous results have indicated that the bilateral cerebral interneuron CC5 mediates the pedal artery shortening that is a component of defensive withdrawal responses involving the head. Current studies suggest that CC5 contributes to aspects of at least six different behaviors: locomotion, head turning, defensive head withdrawal, local tentacular withdrawal, rhythmic feeding, and head lifting. In addition to receiving input from mechanoreceptors in the head, CC5 receives synaptic input during fictive locomotor and feeding programs. Firing of CC5 produces widespread monosynaptic or polysynaptic actions in all ganglia in the animal. CC5 excites presumptive motor neurons for the neck, and its activity can contract neck muscles. The pedal artery shortener motor neuron (PAS), a key excitatory follower cell of CC5, fires during ipsilateral head turning, head withdrawal, tentacle withdrawal, feeding, and locomotion. For all behaviors, except locomotion and biting, responses of PAS were eliminated by cutting the ipsilateral-pleural connective, which interrupts the only direct connection of CC5 to the ipsilateral PAS. The data suggest that CC5 is a multifunctional interneuron that plays different roles during different behaviors. The neuron appears to be involved in producing coordinated movements of the head, involving both somatic and visceral muscles. For some behaviors, or for certain aspects of behaviors, CC5 appears to act as an individual command-like neuron; for other behaviors, CC5 appears to act more as an element of a distributed circuit and is neither necessary nor sufficient for any aspects of the behavior. Key words: command; withdrawal reflex; Aplysia; mechanosensory; feeding; head turning; locomotionAn important conceptual issue in understanding the organization of the nervous system relates to how information is represented. To what extent is information encoded by the activity of individual neurons that perform dedicated functions using local-coding or are neurons always a part of distributed networks using vector coding in which their functional roles are determined by the activity of other neurons in the network (Barlow, 1972;Churchland and Sejnowski, 1992;Morton and Chiel, 1994)? A related question is whether neurons are multifunctional, and growing evidence suggests that indeed multifunctional neurons may be commonly used by the nervous system (Hooper and Moulins, 1989;Lockery and Kristan, 1990;Fetz, 1992;Meyrand et al., 1994;Wu et al., 1994). 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 ani...

Modular Deconstruction Reveals the Dynamical and Physical Building Blocks of a Locomotion Motor Program

“…Consistent with this picture, in further recordings we found that burst firing of pedal nerve 10, correlated with neck contraction (Xin et al, 1996), in turn correlated with a specific portion of the looped trajectory of activity in the ganglion network (Fig. 6C; Supplemental Video 2).…”

“…In some experiments, a separate suction electrode was attached to pedal nerve 10 to continuously monitor the locomotion rhythm (Xin et al, 1996). …”

A spiral attractor network drives rhythmic locomotion

“…Rhythmic locomotion motor programs were elicited using 8V 5ms monophasic pulses delivered at 20Hz for 2.5s via suction electrode to pedal nerve 9. A separate suction electrode was attached to pedal nerve 10 to continuously monitor the locomotion rhythm (Xin et al, 1996). Evoked activity could last for many minutes; our system allowed us to capture a maximum of ≈ 125 s, divided between 30 s of spontaneous activity and 95 s of evoked activity.…”

“…If this putative low-dimensional periodic attractor is the "motor program" for locomotion, then we should be able to decode the locomotion muscle commands from its trajectory. In 3 of the 10 preparations we were able to simultaneously record activity from the P10 nerve that projects to the neck muscles (Xin et al, 1996) for all three evoked population responses. The spiking of axons in this nerve should correspond to the specific neck contraction portion of the cyclical escape locomotion response.…”

Shared versus Specialized Glycinergic Spinal Interneurons in Axial Motor Circuits of Larval Zebrafish

“…There is good evidence from a variety of motor systems that individual neurons are sometimes shared across more than one type of behavior (Morton and Chiel, 1994; Marder and Calabrese, 1996; Xin et al, 1996; Kristan and Shaw, 1997; Berkowitz, 2005; Li et al, 2007). In other cases, however, neurons are not shared, but are specific to only one behavior (Shaw and Kristan, 1997; Berkowitz, 2002).…”