Synaptic And Circuit Mechanisms For Variability Of Motor Programs In Aplysia Feeding Network

When one repeatedly performs the same motor act,these motor acts most commonly show variability between each other,which is represented as variable neuronal firing in invertebrate and vertebrate central nervous system(CNS).Although there is a debate as to its functional significance,variability must originate,at least in part,from mechanisms in the corresponding network.Despite the ubiquity of variability and some molecular and computational studies,little is known about its circuit and synaptic mechanisms.In part,variability both within and between preparations hampers efforts in studying it.We used feeding network of Aplysia,an excellent neurobiology model system to study motor variability.The behavioral and motoneuronal variability has been well characterizedHere we show that from the single pattern-generating circuit,a newly-identified command neuron,CBI-10,that is active during actual feeding behavior,drives motor programs that show more variability in cyclic motoneuronal firing,than programs driven by a previously-identified command neuron(CBI-2).We compared synaptic strengths from the two command neurons to the two central pattern generator interneurons(B34 and B40),and synaptic input of B34 and B40 to the downstream motoneurons(B61/62).We uncover different synaptic strengths from the two command neurons to interneuron B34 and B40,which in turn excite B61/62 differentially.Importantly,stimulation of CBI-10 together with subthreshold depolarization of B34 and B40 makes programs less variable,becoming more similar to programs evoked by CBI-2.Our findings identify synaptic and circuit mechanism for motor variability that the new command neuron(CBI-10)elicits.One is the presence of a pivotal node in the feedforward pathway,pattern-generating neuron B34,which plays a key role in driving the motoneurons(B61/62)strongly and controlling the variability of the motor programs.Second is that the weaker synaptic input from CBI-10 to this pivotal node(B34),so that B34 firing frequency is low.In addition,B34 activity level is inversely correlated with variability of motor programs and has a causal role.Our results establish how variability arises through specific mechanisms in a single feedforward circuit,which may have broad significance because many neural circuits,including cortical circuits,are feedforward and show variability.