Crabs are renowned for their cranky demeanor, but when one considers the extreme conditions under which they must survive, it becomes easier to sympathize with these crotchety crustaceans. One hardship that crabs must endure is changing temperature: a daily swing of 20°C is not unusual for the intertidal zone. Because crabs do not actively maintain a constant internal body temperature, environmental fluctuations pose a serious problem for the crab's nervous system, whose component parts are all uniquely temperature dependent.
A recent study from Wolfgang Stein's lab at Illinois State University, USA, has uncovered some of the neural mechanisms that allow crabs to tolerate capricious weather. Stein, Carola Städele and Stefanie Heigele investigated the effects of temperature on the gastric mill, a neural circuit in the crab stomach whose rhythmic firing controls the chewing movement of three internal ‘teeth’. A convenient feature of the gastric mill is that it continues to produce rhythmic activity even when it is removed from the animal. In this study, the authors used an in vitro preparation to ask how chewing rhythms change when the temperature rises.
Surprisingly, they found that a relatively minor temperature increase, from 10 to 13°C, caused the spontaneous chewing rhythm to completely collapse. When the authors recorded intracellularly from the lateral gastric motoneuron (LG), a key component of the gastric circuit, they found evidence that the temperature change increased the amount of ions that leak across the neuron's membrane, most likely through potassium ‘leak’ channels.
To further test this idea, they manipulated the leak conductance with a technique called dynamic clamp, which allows an electrophysiologist to artificially add or subtract particular ionic conductances while recording from a neuron. When they subtracted the increased leak conductance from the LG neuron at 13°C, they found that the gastric rhythm was restored, consistent with the hypothesis that the temperature-dependent collapse was due to increased leak.
If a temperature increase of just 3°C is enough to disrupt a crab's ability to chew, how does a hot crab ever enjoy a decent meal? To answer this question, the authors recorded extracellularly from the gastric mill in live, chewing crabs. These experiments revealed that the circuit functions over a much wider temperature range in the intact animal, up to 16°C. Thus, under natural conditions, there is active compensation for the temperature-induced collapse of the gastric mill rhythm.
In the second half of the paper, the authors present evidence that robustness to temperature relies on the modulatory commissural neuron (MCN1), a descending neuron that initiates the gastric rhythm. They found that increases in MCN1 input allowed the LG neuron to function at higher temperatures, and bath application of the neuromodulator released by the LG neuron rescued gastric mill rhythms at 13°C.
So, an increase in temperature boosts the leak conductance of the LG neuron and, at the same time, triggers release of a neuromodulator from the MCN1 neuron. This neuromodulator opens a conductance in the LG neuron that compensates for the temperature-dependent increase in leak conductance. Without the intervention of the descending MCN1 neuron, the gastric chewing rhythm would fail at high temperatures, leaving the crab hot and hungry.
It is humbling to consider that the crab has millions of neurons whose intrinsic properties must be constantly fine-tuned to compensate for external temperature fluctuations. The neuromodulatory mechanism elucidated in this paper may exemplify a general solution to this ubiquitous problem.
