The Mauthner neurons have become synonymous with the C start evasive response of fishes. C starts are a two-part movement pattern. First, the fish bends its body so that it has a C-like profile (stage 1) when viewed from above. Second, the fish rapidly accelerates away from its starting position (stage 2). Until recently, it has not been possible to determine the contribution of Mauthner cell activity to the expression of this behavior. In this paper we focus on three of our recent papers that address this issue. Our work combines high-speed digital image analysis of the C start with chronic Mauthner cell and electromyographic recordings, lesions of the Mauthner cells, and stimulation of single Mauthner axons in swimming fishes. This work shows that the firing of the Mauthner cell results in a short-latency body contraction that orients the initial stage of the C start away from the direction of the threatening stimulus. The direction of the escape trajectory, however, is more finely tuned to stimulus angle than can be explained by the firing of just the Mauthner cell and its postsynaptic followers. Precise control of trajectory must, therefore, require participation of other neurons. These neurons together with the Mauthner cell form a system that we term the brain stem escape network. We have identified candidate neurons of this network which can now be studied at the single-cell level. Because of both its accessibility for neurophysiological study and its neuroanatomical simplicity, we assert that the brain stem escape network is a useful preparation for understanding fundamental processes of sensorimotor integration in the brain stem.
As a model for learning how reticulospinal networks coordinate movement, we have analyzed the function of the Mauthner (M-) neurons in the escape response of the goldfish. We used water displacements of 3-6 micron to elicit C-start escape responses. These responses consist of 2 fundamental movements that grade into each other: Stage 1 lasts 15-40 msec and rotates the body 30 degrees-100 degrees about the center of mass; stage 2 is an axial acceleration that moves the center of mass 2-6 cm. Combined, the 2 stages result in trajectory turns ranging from 15 degrees to 135 degrees. Thus, these data show that M-initiated C-starts are not fixed movement patterns. The durations of stage 1 body muscle EMGs were correlated with turn angles achieved during stage 1. Since variable stage 1 EMGs are not seen when the M-cell is triggered by itself, other circuits, independent of the M-cell, must control the extent of the initial turn, and consequently escape trajectory. Furthermore, turning angles of stages 1 and 2 were correlated, allowing escape trajectory to be predicted, on average, 26 msec after movement started. This suggests that the commands for escape trajectory should be organized by the end of stage 1. In concert with this, the time of onset of the stage 2 EMG preceded the stage 2 onset by a range with a mean of 28.4 msec, typically putting the stage 2 command at the beginning of stage 1 movement. Thus, stage 2 initiation does not require motion-dependent feedback. Our findings indicate that the Mauthner cell initiates the first of a series of motor commands that establish the initial left-right decision of the escape sequence from the side of the stimulus, whereas parallel circuits simultaneously organize the command controlling the escape angle.
Predation accounts for substantial mortality during the early development of many fishes. Numerous mechanisms have evolved to avoid predatory attacks. One of these is the C-type fast-start of adult fish responding to an abrupt and unexpected stimulus. This is a short-latency response in which the fish accelerates rapidly away from its position at the time of the attack. In the zebra danio Danio [Brachydanio] rerio, this is one of the earliest behavior patterns to appear during development. It can be readily elicited in embryos as early as 44 h after fertilization, 2 d before normal hatching begins. The behavior pattern is triggered by cells of the reticulospinal system located in the hindbrain. Attacks to the anterior region activate one of a pair of these cells, the Mauthner neurons, whereas attacks to the tail stimulate either a Mauthner neuron or other cells that trigger similar response patterns. In teleosts the early appearance of the reticulospinal escape system emphasizes the probable importance of predatory interactions even for the earliest stages of development. Mechanisms for predator avoidance include a wide range of behavioral and morphological adaptations in larval fish. Many species, such as young rainbow trout Saltno gairdneri, seek out habitats or have behavior patterns that reduce exposure to foraging predators (Carey and Noakes 1981). Despite this, at some time in early life history most species probably encounter other organisms, vertebrates (Hunter and Kimbrell 1981) or invertebrates (Lillelund and Lasker 1971; Theilacker and Lasker 1974; Westernhagen and Rosenthal 1976; Bailey and Batty 1983), attempting to make a predatory capture. These are situations in which the predator has selected an individual prey and is within capture range. Because of the small size of fish larvae and many of their predators, the capture range may vary from a few centimeters to less than a millimeter. Detection of the predator and a fast reaction time are crucial factors for survivability (Webb 1976). In a wide variety of fishes, the decision to respond, and the entire escape movement, all take place in less than a tenth of a second (Eaton et al. 1977a). Typical reaction times are a few tens of milliseconds, and escape accelerations are several times gravity (Eaton and Hackett 1984). These performance domains approach the limits of biological system capability; strong selective pressures probably shaped the evolution of this behavior.Fish possess a variety of specializations--behavioral, physiological, and anatomical--tuned to the requirements of rapid avoidance. Associated with the peak performance necessary for escape are many conspicuous features, like fast-conduct-ing neural circuits, that have figured prominently in the historical discovery of basic cellular processes in development and physiology. Correlated with this work is the discovery that specialized escape behavior and its underlying neural systems are widespread among teleosts and function from the earliest stages of development, even before emergenc...
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