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The Journal of Neuroscience, July 2, 2003, 23(13):5617-5626

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Central Cellular Mechanisms Underlying Temperature-Dependent Changes in the Goldfish Startle-Escape Behavior

Thomas Preuss and Donald S. Faber

Albert Einstein College of Medicine, Department of Neuroscience, New York, New York 10461

Activation of auditory afferents on the lateral dendrite of the Mauthner (M)-cell triggers an escape response (C-start) in goldfish. To study distinct behavioral changes and their physiological correlates on a cellular level we examined the effect of acute changes of temperature on M-cell membrane properties and intracellular responses to sound clicks and on C-start kinematics and behavior, focusing on threshold and initial escape direction, two properties determined on the M-cell level. Cooling slowed C-start motor performance, increasing response latency and decreasing peak velocity and peak acceleration, but increased the probability of triggering the escape. In addition, the likelihood of escapes in an inappropriate direction (e.g., responses toward the stimulus instead of away from it) increased at low temperatures. On a cellular level, cooling caused a distinct increase in input resistance of the M-cell and in the dendritic space constant for the auditory-evoked synaptic potentials. Moreover, cooling decreased the magnitude and delayed the onset of feedforward inhibition of the M-cell. These temperature-induced changes in the network and in the intrinsic M-cell properties combine to support behavioral hyperexcitability, but apparently also alter the directional decision-making process during an escape. More generally, our results illustrate that the balance between excitatory and inhibitory influences can determine the expression of a behavior and its modification and at the same time underline the significance of temperature for nervous system function and behavior.

Key words: dendritic cable properties; auditory-evoked response; excitatory/inhibitory balance; kinematics; neural temperature effects; escape behavior; neuroethology; Mauthner cell

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Received Mar. 4, 2003; revised Apr. 7, 2003; accepted Apr. 9, 2003.

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