We describe three slow muscles that responded to low-frequency modulation of a high-frequency neuronal input and, consequently, could express the motor patterns of neural networks whose neurons did not directly innervate the muscles. Two of these muscles responded to different frequency components present in the same input, and as a result each muscle expressed the motor pattern of a different, non-innervating, neural network. In an analogous manner, the distinct dynamics of the multiple intracellular processes that most cells possess may allow each process to respond to, and hence differentiate among, specific frequency ranges present in broad-band input.

In several systems, including some well studied invertebrate "model" preparations, rapid, rhythmic inputs drive slow muscles. In this situation muscle contractions can summate temporally between motor neuron bursts, tonically contract, and low-pass filter broad-band input. We have investigated how the muscles innervated by each motor neuron type of the rapid, rhythmic (cycle period, approximately 1 sec) lobster pyloric network respond when driven by previously recorded in vitro pyloric network activity from intact stomatogastric nervous systems. Under these conditions the much slower gastric mill and cardiac sac networks of the stomatogastric nervous system are also active and modify pyloric activity. All of the muscles show pyloric timed phasic contractions that ride on a sustained tonic contraction; muscle activity can range from being almost completely phasic to almost completely tonic. The modifications of pyloric neuron activity induced by gastric mill (cycle period, approximately 10 sec) activity result in some pyloric muscles showing prominent, gastric mill-timed, changes in either phasic or tonic contraction amplitude. The strong modification of pyloric neuron activity induced by cardiac sac (cycle period, approximately 60 sec) activity alters the contractions of all pyloric muscles. These changes are sufficient that for some muscles, in some preparations, the primary muscle output is cardiac sac-timed. This is the first work to examine the motor responses of all pyloric muscle classes to spontaneous stomatogastric activity and shows that the pyloric motor pattern is a complex combination of the activities of three neural networks, although only one (the pyloric) innervates the muscles.

It has long been known that gastric mill network activity (cycle period 5-10 s) alters pyloric network output (cycle period approximately 1 s), but these effects have not been quantified. Many pyloric muscles extract gastric mill timed variations in pyloric motor neuron firing, and consequently produce gastric mill timed movements even though no gastric mill neurons innervate them. Determining pyloric behavior therefore requires detailed description of gastric mill effects on pyloric neural output. Pyloric muscle activity correlates well with motor neuron overall spike frequency (OSF, burst spike number divided by cycle period). We quantified OSF variation of all pyloric neurons as a function of time into the gastric mill cycle [as measured from the beginning of Gastric Mill (GM) neuron bursts] in the lobster, Panulirus interruptus. No repeating pattern within individual gastric mill cycles of Lateral Pyloric (LP) and Ventricular Dilator (VD) neuron OSF was visually apparent. Averaged data showed that VD and LP neuron OSF decreased (approximately 0.5 and 1.5 Hz, respectively) at the beginning of each gastric mill cycle. Visually apparent patterns of OSF waxing and waning within each gastric mill cycle were present for the Inferior Cardiac (IC), Pyloric Dilator (PD), and Pyloric (PY) neurons. However, when averaged as a function of phase or delay in the gastric mill cycle, the average changes were smaller than those in individual gastric mill cycles because when the OSF variations occurred varied considerably in different gastric mill cycles. We therefore used a "pattern-based" analysis in which an identifying characteristic of each neuron's repeating OSF variation pattern was defined as pattern pyloric cycle zero. The pyloric cycles in each repetition of the OSF variation pattern were numbered relative to the zero cycle, and averaged to create an average OSF variation profile. The zero cycle delays relative to GM neuron burst beginning were then averaged to determine when in the gastric mill cycle the profile occurred. This technique preserved the full extent of pyloric neuron OSF changes. Maximum PY neuron OSF occurred within the GM neuron burst, whereas maximum IC and PD neuron OSF occurred during the GM neuron interburst interval. Despite these changes, pyloric cycling did not phase lock with gastric mill activity, nor were an integer number of pyloric cycles present in each gastric mill cycle. In addition to providing data necessary to predict pyloric movement, this work shows how pattern-based analysis can successfully quantify interactions between nonphase-locked networks.

Cardiac sac network activity (cycle period tens of seconds to minutes) has long been known to alter pyloric network activity (cycle period approximately 1 s), but these effects have not been quantified. Some pyloric muscles extract cardiac sac timed variations in pyloric motor neuron firing, and consequently produce cardiac sac timed movements even though no cardiac sac neurons innervate them. Determining pyloric behavior therefore requires detailed description of cardiac sac effects on pyloric neural output. Pyloric muscle activity correlates well with motor neuron overall spike frequency (OSF, number of spikes per burst divided by cycle period). We therefore quantified the effects of cardiac sac activity on the OSF of all pyloric neurons in the lobster, Panulirus interruptus. The ventricular dilator (VD) neuron had a biphasic response, with its OSF first increasing and then decreasing during cardiac sac bursts. Lateral pyloric (LP) neuron OSF decreased during cardiac sac activity. The pyloric (PY) neurons had two responses, with OSF either decreasing or increasing just after the beginning of cardiac sac activity. The pyloric dilator (PD) neurons had a triphasic response, with OSF increasing slightly at the beginning of cardiac sac activity, decreasing during the cardiac sac burst, and strongly increasing after cardiac sac activity ended. The inferior cardiac (IC) neuron had a biphasic response, with OSF decreasing at the beginning of cardiac sac activity and strongly increasing when cardiac sac activity ceased. These data provide the quantitative description of cardiac sac effects on pyloric activity necessary to predict pyloric movement from pyloric neural output.