The caridoid escape reaction, also known as lobstering or tail-flipping, is an innate escape behavior in marine and freshwater eucarid crustaceans such as lobsters, krill, shrimp and crayfish.
The reaction, most extensively researched in crayfish, allows crustaceans to escape predators through rapid abdominal flexions that produce powerful thrusts that make the crustacean quickly swim backwards through the water and away from danger. The type of response depends on the part of the crustacean stimulated, but this behavior is complex and is regulated both spatially and temporally through the interactions of several neurons.
Discovery of the first command neuron-mediated behavior
In 1946, C. A. G. Wiersma first described the tail-flip escape in the crayfish Procambarus clarkii and noted that the giant interneurons present in the tail were responsible for the reaction. The aforementioned neuronal fibres consist of a pair of lateral giant interneurons and a pair of medial giant interneurons, and Wiersma found that stimulating just one lateral giant interneuron (LG or LGI) or one medial giant interneuron (MG or MGI) would result in the execution of a tail flip. Wiersma and K. Ikeda then proposed the term "command neuron" in their 1964 publication, and applied it to the giant interneuron's ability to command the expression of the escape response. This was the first description of a command neuron-mediated behavior and it indicated that the depolarization of a neuron could precipitate complex innate behaviors in some organisms. Chapter 7: Escape Behavior in Crayfish
This concept was further fleshed out with more specific and stringent conditions in 1972 when Kupfermann and Weiss published The Command Neuron Concept. The paper stated that command neurons were neurons (or small sets of neurons) carrying the entire command signal for a natural behavioral response. According to the authors, command neurons were both necessary and sufficient in the production of a behavioral response. The concept of command neuron-mediated behaviors was both ground breaking and controversial, since determining command neuron-mediated behaviors was a problematic process due to difficulties in understanding and interpreting anatomical and behavioral data.
Research with crayfish
Behavioral neurobiologists in the field of neuroethology have researched this behavior extensively for over fifty years in the crayfish species Procambarus clarkii. Based on studies of P. clarkii it was discovered that the tail-flip mechanism is characterized by a decisive, all-or-nothing quality that inhibits all unnecessary behaviors while generating a fixed action pattern for escape swimming. The type of escape response depends on the region of the crayfish that is stimulated but all forms require abdominal contractions. When a strong, unpleasant tactile stimulus is presented, such as a burst of water or the prod of a probe, a stereotyped behavior occurs in which the muscular tail and wide tail fan region of the telson are used like a paddle to propel the crustacean away from harm using powerful abdominal flexions. The entire process occurs in a fraction of a second as movements are generated within two hundredths of a second (20 milliseconds) from the original trigger stimulus and the period of latency after a flexion is a hundredth of a second (10 milliseconds). Finally, the caridoid escape reflex requires that neurons be able to complete the arduous task of synchronizing the flexion of several abdominal segments. The speed, coordination, and decisiveness of the process seem to be the main attributes to its success.
Anatomy involved
Like other decapod crustaceans, the crayfish possesses a hard, segmented exoskeleton that reflects muscular and neural segmentation. The anterior portion of the crayfish is the cephalothorax region. The region rostral to the cephalic groove, which separates the head and thorax region, is characterized by the presence of eyes, antennae and claws while the region caudal contains four pairs of walking legs. This is the crayfish's primary mode of locomotion. The abdominal section of the crayfish is divided into seven segments. These segments are flexibly interconnected, forming the tail. Normally, the tail is held in an extended position to aid in maneuvering and balancing. The first five segments are similar and the two terminal segments are modified into a tail fan, a region with high surface area that acts as the blade of a paddle in the escape response. This region contains the telson. The abdominal segments contain swimmerets, which aid in swimming.
The anterior five segments of the crayfish house the massive flexor and extensor muscles. Six abdominal ganglia run down the entire length of the abdomen and communicate with one another through projections. The first five abdominal segments each have their own ganglion, that contains three roots with outward projections. The first has mixed sensory and motor nerves innervating swimmerets while the second has sensory and motor neurons that innervate the extensor muscles, while the third root contains only motor neuron projections that extend into the flexor muscles. The last segment contains the fusion of two ganglia. The ganglia here also receive sensory input from the sensitive hairs on the tail fan.
Each ganglion contains the body of one motor giant neuron (MoG), powerful and large bodied motor neurons whose projections innervate the five fast flexor (FF) muscles found in a segment and interact with them through chemical synapses. The ganglia also contain two sets of giant axons known as the lateral giant neurons and the medial giant neurons. These interneurons play important roles in escape swimming. Their large diameter allows for rapid conduction since there is less current leakage. Their projections extend through the third root in each ganglion, and Furshpan and Potter found that the synapses they subsequently made with the MoG passed depolarizing currents in a direct and unidirectional manner. These electrical synapses account for the speed of the escape mechanism and display some features of chemical synapses such as LTP and LTD. Variations in escape response characteristic depend on the location where the crayfish body is prodded or attacked and also depend on which of the giant neurons is stimulated.
Response variants and their circuitry
Medial giant-mediated escape
The medial giants innervate the entire ventral nerve cord. Their cell bodies and dendrites begin in the brain and collect sensory information presented by visual and tactile stimuli. These fibers terminate in the last abdominal segment. The response is triggered by abrupt tactile stimuli to the head or alarming visual stimuli. This results in the firing of all motor giant (MoG) neurons and the flexion of all the phasic fast flexor (FF) muscles in the abdomen, which rapidly curls the tail fan and last three segments underneath the crayfish. This produces a thrust that directs water towards the offending stimulus while propelling the crayfish directly backward. This behavior is then followed by the extension of the tail, which prepares it for swimming or the execution of another tail-flip.
Unfortunately, this variant of the tail-flip escape has not been extensively studied. Further studies should focus on this escape variant, paying special attention to exactly how visual information is processed and then converted into neuronal signals that produce a tail flip response.
Non-giant escape
Less abrupt or gradually intensifying stimuli evoke locomotion behavior similar to that seen in giant interneuron-mediated behaviors. However, the movements are less stereotyped and do not appear to occur in an all or nothing manner. They are so named because they lack the involvement of the giant interneurons, most likely because they do not produce depolarizations in the sensory neurons that are above the thresholds required to initiate these behaviors. Instead they involve one or a few of the smaller neurons innervating the tail. The latency periods for these escape mechanisms are longer, ranging from 80 to 500 ms. However, this slower swimming behavior allows for flexibility, since the crayfish can use visual stimuli and steer itself in a selected direction.
Non-giant escape often occurs during situations where lateral or medial giant-mediated escape may not be beneficial or during times where those behaviors are suppressed. This allows the crayfish to attack offenders, escape during feeding, or wriggle free when it has been restrained by the carapace.
Non-giant escape circuitry was found to be activated more during frontal attacks, but was rarely involved in the initial escape during a rear attack. Non-giant escape is often used after an initial giant interneuron-mediated tail flip. Compared to MG escape, the potentials produced in the MoG neurons by non-giant circuitry have lower amplitudes and longer durations while the recordings in the FF muscles are more erratic and have smaller amplitudes since they receive smaller EPSPs from the MoGs. So while it is hard to observe differences in MG and non-escapes, this property can be used to distinguish the two.
Lateral giant-mediated escape
The lateral giant (LG)-mediated escape mechanism is the most extensively analyzed form of the tail flip. The LG is not actually one neuron, but rather a group of closely associated neurons arranged end to end and connected by electrical synapses (also called septate synapses). As a result, the LGI functions as one giant, continuous neuron, such as the MG. The LGI's large diameter and the efficiency and speed of electrical synapses, make the LGI-mediated escape especially rapid and effective. The LGI only innervates the first three rostral segments of the tail and is activated within 10 ms from when a mechanical stimulus is presented to the abdomen. When flexion occurs, only the first three segments flex and the tail fan is not directed under the body and forward but rather straight down. The unflexed segments increase the length of the paddle. The result is the rear end of the animal is directed upward and forward causing the animal to tumble or somersault forward. The tail is then rapidly extended, and this is usually followed by directed swimming.
The LGI is one of the few examples of a true command neuron. It passes the necessity and sufficiency principle put forward by Kupfermann and Weiss. Wiersma's initial experiments showed that direct stimulation of the LGI was a sufficient release for the tail flip. In 1981, it was Olson and Krasne who showed that the LGI fulfilled the condition of necessity, because when spikes were inhibited in the LGI through introducing a hyperpolarizing current, no motor activity was produced in response to a stimulus that would have originally elicited the tail flip.
The LGI contains the following three phases, occurring over the span of about 100 ms:
1 – Flexion production