Temperature sensitivity of the pyloric neuromuscular system and its modulation by dopamine

We report here the effects of temperature on the p1 neuromuscular system of the stomatogastric system of the lobster (Panulirus interruptus). Muscle force generation, in response to both the spontaneously rhythmic in vitro pyloric network neural activity and direct, controlled motor nerve stimulation, dramatically decreased as temperature increased, sufficiently that stomach movements would very unlikely be maintained at warm temperatures. However, animals fed in warm tanks showed statistically identical food digestion to those in cold tanks. Applying dopamine, a circulating hormone in crustacea, increased muscle force production at all temperatures and abolished neuromuscular system temperature dependence. Modulation may thus exist not only to increase the diversity of produced behaviors, but also to maintain individual behaviors when environmental conditions (such as temperature) vary

Dopamine allows the neuromuscular system to generate greater force at cold temperatures and continue functioning at warm temperatures.

<p>(A) Data from six motor nerve stimulation experiments (closed circles, control saline; open circles, dopamine; matching color lines are data from the same experiment; all animals housed at 15°C). Where present, solid lines show that linear fits to the data were significant. (B) Data for each experiment were binned (1°C) and mean contraction force was determined for each bin. Dopamine differed from control and wash conditions both in amplitude and in temperature sensitivity (present in control and wash, absent in dopamine). See text for statistical details.</p

Changing available dissolved oxygen does not affect temperature sensitivity.

<p>The preparation was initially perfused with cold, oxygenated saline (top trace) and then switched (arrow) to cold saline containing at least 3 fold less dissolved oxygen. The muscle showed no change in activity (bottom trace) when the reduced oxygen saline was introduced. However, the temperature sensitivity remained and was still reversible despite the much lower oxygen availability. The periodic large decreases in muscle force every 75–100 s are due to the activity of another, much more slowly cycling, stomatogastric network, the gastric mill, which greatly reduces lateral pyloric neuron activity during one phase of gastric mill activity <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0067930#pone.0067930-Morris4" target="_blank">[13]</a>, <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0067930#pone.0067930-Thuma2" target="_blank">[15]</a>.</p

The lobster p1 neuromuscular system is temperature-sensitive.

<p>(A) As temperature (top trace) was decreased the force of muscle contraction (middle trace) increased. The activity of the nerve containing the LP neuron input to the muscle is shown in the bottom trace. (B) and (C) Time expansion from (A) showing muscle force (top trace) and neural input (bottom trace) at 9°C and 15°C. Arrows show that two LP neuron bursts chosen for having essentially identical characteristics induced very different muscle contraction amplitudes at the two temperatures. Inset in (C) is muscle force at an expanded scale to show that even at warm temperatures each motor neuron burst continued to induce (very small) muscle contractions.</p

Dopamine blocks temperature sensitivity in an isolated, rhythmically stimulated neuromuscular preparation.

<p>(A) A neuromuscular preparation that has been isolated from the spontaneous activity of the pyloric neural network by severing the lvn. Contractions instead elicited by direct motor nerve stimulation with unvarying input (10 spikes at 27 Hz). Muscle contraction amplitude still declined dramatically in warmer saline. This animal had been acclimated to 15°C for 48 hrs, and thus these data also show that neuromuscular temperature sensitivity is independent of animal housing temperature. (B) Adding dopamine (10⁻⁵) to the saline increased force generation at colder temperatures and allowed the neuromuscular system to continue functioning at warmer temperatures. (C) The dopamine effect reversed upon wash. (D) Dopamine also maintained contraction amplitude in neuromuscular systems from animals held in 9°C aquaria for 48 hrs before the experiment. Data in panels A, B, C all from same animal.</p