1996Journal of NeuroscienceOpen access

Interactions between the neural networks for escape and swimming in goldfish

K. R. Svoboda, JR Fetcho

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Abstract

Interactions between neural networks for different motor behaviors occur frequently in nature; however, there are few vertebrate models for studying these interactions. One potentially useful model involves the interactions between escape and swimming behaviors in fish. Fish can produce escape bends while swimming, using some of the same axial muscles for both behaviors. Here we study the interactions between escape and swimming in a paralyzed goldfish preparation in which we can activate the networks for both behaviors. Fictive swimming was elicited by electrical stimulation in the midbrain locomotor region. During the swimming, we fired a single action potential in the reticulospinal Mauthner (M) cell, which initiates the escape behavior (Zottoli, 1977). Firing the M cell overrode the swimming motor output to produce an output appropriate for escape regardless of the phase of swimming at which it was fired. The M cell also could reset the swimming rhythm dramatically in a way that led to a smooth transition from an escape bend to one side into subsequent swimming. Both the override and reset supported predictions based on previous studies of the organization of the M-cell network. They apparently allow for a well coordinated motor output when a fish must produce an escape while swimming. The potent effects of one action potential in a single, identifiable reticulospinal neuron make this an attractive model system for future studies of the cellular basis of interactions between descending pathways and spinal rhythm-generating networks.

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Interactions between neural networks for different motor behaviors occur frequently in nature; however, there are few vertebrate models for studying these interactions. One potentially useful model involves the interactions between escape and swimming behaviors in fish. Fish can produce escape bends while swimming, using some of the same axial muscles for both behaviors. Here we study the interactions between escape and swimming in a paralyzed goldfish preparation in which we can activate the networks for both behaviors. Fictive swimming was elicited by electrical stimulation in the midbrain locomotor region. During the swimming, we fired a single action potential in the reticulospinal Mauthner (M) cell, which initiates the escape behavior (Zottoli, 1977). Firing the M cell overrode the swimming motor output to produce an output appropriate for escape regardless of the phase of swimming at which it was fired. The M cell also could reset the swimming rhythm dramatically in a way that led to a smooth transition from an escape bend to one side into subsequent swimming. Both the override and reset supported predictions based on previous studies of the organization of the M-cell network. They apparently allow for a well coordinated motor output when a fish must produce an escape while swimming. The potent effects of one action potential in a single, identifiable reticulospinal neuron make this an attractive model system for future studies of the cellular basis of interactions between descending pathways and spinal rhythm-generating networks.

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Available abstract

Interactions between neural networks for different motor behaviors occur frequently in nature; however, there are few vertebrate models for studying these interactions. One potentially useful model involves the interactions between escape and swimming behaviors in fish. Fish can produce escape bends while swimming, using some of the same axial muscles for both behaviors. Here we study the interactions between escape and swimming in a paralyzed goldfish preparation in which we can activate the networks for both behaviors. Fictive swimming was elicited by electrical stimulation in the midbrain locomotor region. During the swimming, we fired a single action potential in the reticulospinal Mauthner (M) cell, which initiates the escape behavior (Zottoli, 1977). Firing the M cell overrode the swimming motor output to produce an output appropriate for escape regardless of the phase of swimming at which it was fired. The M cell also could reset the swimming rhythm dramatically in a way that led to a smooth transition from an escape bend to one side into subsequent swimming. Both the override and reset supported predictions based on previous studies of the organization of the M-cell network. They apparently allow for a well coordinated motor output when a fish must produce an escape while swimming. The potent effects of one action potential in a single, identifiable reticulospinal neuron make this an attractive model system for future studies of the cellular basis of interactions between descending pathways and spinal rhythm-generating networks.

Key concepts: Mauthner cell, Escape response, Neuroscience, Midbrain, Reset (finance), Fish <Actinopterygii>, Rhythm, Vertebrate

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