Mauthner neurons and the teleost fast start

When a sharp tap is delivered to the side of an aquarium, the fish inside exhibit a characteristic startle response consisting of a brisk swivelling movement that displaces the fish sideways by a small amount. In natural circumstances, this is an effective escape movement that enables the animal to dodge the strike of a predator. The key neuron in this startle response is called the Mauthner neuron; there is one of these neurons on each side of the brain of most species of fish and of amphibians. Most studies of these neurons have been made in goldfish and zebra fish. Because of the exceptionally large size of Mauthner neurons, it has been possible to study them in both dissected preparations and intact animals; these studies provide one of the few cases in vertebrates in which a clear causal relationship has been established between activity in a particular neuron and performance of a specific behaviour pattern. The way the Mauthner neuron operates shows a number of instructive parallels with the crayfish lateral giant neuron.

In teleost fish, the startle movement initiated by a Mauthner neuron is known as a fast start, and consists of a stereotyped sequence of movements that occur in three stages. In the initial stage, the trunk muscles contract all along one side of the body so that the animal assumes a C-like shape with the head and tail bent to the same side. A number of other actions are also initiated, such as closing the mouth, drawing in the eyes and extending the fins. During the second stage, muscle contractions proceed down the other side of the body so that the tail straightens. These first two stages result in a sudden acceleration that propels the animal in a direction that is determined by the extent of the body bend in the first stage and displaces the fish by about one body length. The third stage consists of normal swimming movements, or sometimes coasting, which carries the fish further away.

Figure 3.8 The Mauthner neuron in teleost fish. (a) The general location of the bilateral pair of Mauthner neurons (M) shown schematically for a larval zebra fish (Brachydanio). (b) The right Mauthner neuron is shown in a thick, transverse section of the hindbrain at the level of the eighth cranial nerve, together with the inputs from the lateral line and acoustico-vestibular systems. The output of the Mauthner axon to the spinal motor neurons is shown in a thick transverse section of the spinal cord. (c) The Mauthner neuron of an adult goldfish (Carausius), reconstructed from transverse sections of a cell injected with intracellular dye. (a modified after Prugh, Kimmel & Metcalfe, 1982; b modified after Kimmel & Eaton, 1976; c redrawn after Zottoli, 1978.)

Figure 3.8 The Mauthner neuron in teleost fish. (a) The general location of the bilateral pair of Mauthner neurons (M) shown schematically for a larval zebra fish (Brachydanio). (b) The right Mauthner neuron is shown in a thick, transverse section of the hindbrain at the level of the eighth cranial nerve, together with the inputs from the lateral line and acoustico-vestibular systems. The output of the Mauthner axon to the spinal motor neurons is shown in a thick transverse section of the spinal cord. (c) The Mauthner neuron of an adult goldfish (Carausius), reconstructed from transverse sections of a cell injected with intracellular dye. (a modified after Prugh, Kimmel & Metcalfe, 1982; b modified after Kimmel & Eaton, 1976; c redrawn after Zottoli, 1978.)

The large cell body and two primary dendrites of a Mauthner neuron are located in the hind brain (Fig. 3.8). The axon crosses to the opposite side of the brain before descending the nerve cord to contact motor neurons of trunk muscles. This basic anatomy was described by Bartelmez (1915), who first suggested that it was involved in startle behaviour, although for several decades after that it was thought that the Mauthner neuron is involved in normal swimming movements. The role of the neuron in startle behaviour was firmly established when recordings from the neuron were correlated with movements in freely moving animals - spikes in a Mauthner neuron can be identified unambiguously in extracellular recordings because their waveform provides a characteristic signature. When a spike is recorded from a Mauthner neuron in response to a sudden sound, it is always immediately followed by a large muscle potential in the trunk muscles on the side of the body opposite to the Mauthner neuron cell body, and the fish performs a fast start (Fig. 3.9 a).

The precise timing of the Mauthner spike in relation to the stages of the fast start is clarified by using an implanted electrode in conjunction with high-speed filming of the response (Fig. 3.9b). This method shows that the average delay from a stimulus to a Mauthner spike is about 6 ms. There is a further delay of about 2 ms until the muscle potential starts and then a delay of 6-10 ms until the muscle develops sufficient tension for actual movement to begin. The speed of this startle response is comparable to that of the crayfish tail flip, which is not surprising as both are natural responses for evading the strike of a predator. Another parallel with the crayfish startle system is that only a single spike occurs in the Mauthner neuron, and this precedes the initial C-like bend. Mauthner spikes do not accompany the second stage or subsequent swimming, which must therefore be due to the activity of other interneurons acting in parallel with the Mauthner neuron.

The Mauthner neuron on the side closest to the stimulus is the only one that produces a spike and, because this excites the contralateral musculature, the initial C-like turn is made to the side away from the stimulus. The size of this initial turn is not constant but varies with the angle of the threatening stimulus with respect to the fish. This is shown by dropping a metal ball on to the water near the goldfish and analysing high-speed films of the resulting startle response. In this experiment, the angle through which the fish has turned by the end of stage one is inversely proportional to the direction of the impact of the ball (Eaton & Emberley, 1991). When the startle response is filmed in goldfish with electrodes implanted in the trunk musculature (as in Fig. 3.9 a), the results show that progressively larger turns in stage one are correlated with progressively longer and more complex muscle potentials. The fish is evidently controlling how far it turns by varying the activity of motor neurons supplying the trunk musculature.

Figure 3.9 Activity of the Mauthner neuron during startle behaviour. (a) A goldfish in an aquarium with electrodes implanted for recording from one Mauthner neuron and from both left and right trunk muscles in a freely moving animal. The stimulus is delivered by a loudspeaker (at left) and monitored by a hydrophone (at right). (b) Typical recording of a startle response to a sound stimulus (bottom trace, On/Off). The brain electrode (top trace) picks up the Mauthner spike (M) and also the prominent potential that spreads from the trunk musculature. The two myogram electrodes (middle traces) show that this muscle potential originates from the contralateral muscles (contra) and not the ipsilateral muscles (ipsi). (c) Simultaneous recording with electrodes implanted in the brain and highspeed filming in dorsal view (representative silhouettes at bottom) serves to establish the precise timing of the Mauthner spike in startle behaviour. (a and b modified after Zottoli, 1977; c modified after Eaton, Lavender & Wieland, 1981.)

Figure 3.9 Activity of the Mauthner neuron during startle behaviour. (a) A goldfish in an aquarium with electrodes implanted for recording from one Mauthner neuron and from both left and right trunk muscles in a freely moving animal. The stimulus is delivered by a loudspeaker (at left) and monitored by a hydrophone (at right). (b) Typical recording of a startle response to a sound stimulus (bottom trace, On/Off). The brain electrode (top trace) picks up the Mauthner spike (M) and also the prominent potential that spreads from the trunk musculature. The two myogram electrodes (middle traces) show that this muscle potential originates from the contralateral muscles (contra) and not the ipsilateral muscles (ipsi). (c) Simultaneous recording with electrodes implanted in the brain and highspeed filming in dorsal view (representative silhouettes at bottom) serves to establish the precise timing of the Mauthner spike in startle behaviour. (a and b modified after Zottoli, 1977; c modified after Eaton, Lavender & Wieland, 1981.)

However, direct electrical stimulation of the Mauthner neuron consistently results in a short and simple muscle potential. Hence, the size of the C-like turn must be controlled by other interneurons that are active in parallel with the Mauthner neuron (Eaton, Di Domenico & Nissanov, 1991).

Figure 3.10 Sensory input to the Mauthner neuron. (a) Schematic representation of input to the lateral dendrite from the eighth cranial nerve, showing receptors with direct electrical (—|) synapses onto the Mauthner neuron (M) and those with indirect chemical synapses (—by way of sensory interneurons (SI). (b) Intracellular recording from the distal end of the lateral dendrite, as indicated in (a), showing two superimposed records. Following electrical stimulation of the receptor axons, a compound EPSP is recorded, with an early component (a) due to the electrical synapse and a later component (p) due to the chemical synapses. In one of the records, the latter triggers a spike, which is small in size because it has spread passively from the spike-initiating zone to the recording site. (b modified after Diamond, 1968.)

Figure 3.10 Sensory input to the Mauthner neuron. (a) Schematic representation of input to the lateral dendrite from the eighth cranial nerve, showing receptors with direct electrical (—|) synapses onto the Mauthner neuron (M) and those with indirect chemical synapses (—by way of sensory interneurons (SI). (b) Intracellular recording from the distal end of the lateral dendrite, as indicated in (a), showing two superimposed records. Following electrical stimulation of the receptor axons, a compound EPSP is recorded, with an early component (a) due to the electrical synapse and a later component (p) due to the chemical synapses. In one of the records, the latter triggers a spike, which is small in size because it has spread passively from the spike-initiating zone to the recording site. (b modified after Diamond, 1968.)

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