Brainstem reticulospinal neurons (RSNs) serve as the major descending system in vertebrate sensorimotor integration. One of the paired RSNs in zebrafish, the Mauthner (M) cell, is thought to initiate fast escape from sudden noxious stimuli. Two other paired RSNs, morphologically homologous to the M-cell, are also suggested to play key roles in controlling fast escape. However, the relationship among activities of the M-cell and its homologs during fast escape and the sensory inputs that elicit escape via their activation are unclear. We have monitored hindbrain RSN activity simultaneously with tail flip movement during fast escape in zebrafish. Confocal calcium imaging of RSNs was performed on larvae rostrally embedded in agar but with their tails allowed to move freely. Application of a pulsed waterjet to the otic vesicle (OV) to activate acousticovestibular input elicited contralateral fast tail flips with short latency and an apparent Ca 2ϩ increase, reflecting a single action potential, in the ipsilateral M-cell (M-escape). Application of waterjet to head skin for tactile stimulation elicited fast escapes, but onset was delayed and the M-cell did not fire (non-M-escape). After eliminating either the M-cell or OV, only non-M-escape was initiated. Simultaneous high-speed confocal imaging of the M-cell and one of its homologs, MiD3cm, revealed complementary activation during fast escape: MiD3cm activity was low during M-escape but high during non-M-escape. These results suggest that M-cell firing is necessary for fast escape with short latency elicited by acousticovestibular input and that MiD3cm is more involved in non-M-escape driven by head-tactile input.

In teleost fish, the Mauthner (M) cell, a large reticulospinal neuron in the brainstem, triggers escape behavior. Spinal commissural inhibitory interneurons that are electrotonically excited by the M-axon have been identified, but the behavioral roles of these neurons have not yet been addressed. Here, we studied these neurons, named CoLo (commissural local), in larval zebrafish using an enhancer-trap line in which the entire population of CoLos was visualized by green fluorescent protein. CoLos were present at one cell per hemi-segment. Electrophysiological recordings showed that an M-spike evoked a spike in CoLos via electrotonic transmission and that CoLos made monosynaptic inhibitory connections onto contralateral primary motoneurons, consistent with the results in adult goldfish. We further showed that CoLos were active only during escapes. We examined the behavioral roles of CoLos by investigating escape behaviors in CoLo-ablated larvae. The results showed that the escape behaviors evoked by sound/vibration stimuli were often impaired with a reduced initial bend of the body, indicating that CoLos play important roles in initiating escapes. We obtained several lines of evidence that strongly suggested that the impaired escapes occurred during bilateral activation of the M-cells: in normal larvae, CoLo-mediated inhibitory circuits enable animals to perform escapes even in these occasions by silencing the output of the slightly delayed firing of the second M-cell. This study illustrates (1) a clear example of the behavioral role of a specialized class of interneurons and (2) the capacity of the spinal circuits to filter descending commands and thereby produce the appropriate behavior.

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SummaryThe coding of stimulus information into patterns of spike times occurs widely in sensory systems. Determining how temporally coded information is decoded by central neurons is essential to understanding how brains process sensory stimuli. Mormyrid weakly electric fishes are experts at time coding, making them an exemplary organism for addressing this question. Mormyrids generate brief, stereotyped electric pulses. Pulse waveform carries information about sender identity, and it is encoded into submillisecond-to-millisecond differences in spike timing between receptors. Mormyrids vary the time between pulses to communicate behavioral state, and these intervals are encoded into the sequence of interspike intervals within receptors. Thus, the responses of peripheral electroreceptors establish a temporally multiplexed code for communication signals, one consisting of spike timing differences between receptors and a second consisting of interspike intervals within receptors. These signals are processed in a dedicated sensory pathway, and recent studies have shed light on the mechanisms by which central circuits can extract behaviorally relevant information from multiplexed temporal codes. Evolutionary change in the anatomy of this pathway is related to differences in electrosensory perception, which appears to have influenced the diversification of electric signals and species. However, it remains unknown how this evolutionary change relates to differences in sensory coding schemes, neuronal circuitry and central sensory processing. The mormyrid electric communication pathway is a powerful model for integrating mechanistic studies of temporal coding with evolutionary studies of correlated differences in brain and behavior to investigate neural mechanisms for processing temporal codes.Key words: sub-millisecond timing differences, duration tuning, interval tuning, coincidence detection, anti-coincidence detection, delay line, temporal filter, weakly electric fish, electric organ discharge. Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Japan *Author for correspondence (carlson.bruce@wustl.edu) THE JOURNAL OF EXPERIMENTAL BIOLOGY 2366 that links changes in neural circuitry to differences in behavior. From the perspective of the central nervous system, there is no difference between the electrosense and other modalities -all stimuli are represented as patterns of spiking. Therefore, the mechanisms by which mormyrids process temporally coded information are relevant to understanding basic principles for how any neural circuit can solve this problem.Electric signals in mormyrid fishes communicate sender identity and behavioral state Two components of electrocommunication: EOD and IPI Mormyrids produce an electric organ discharge (EOD) to communicate and actively sense their environment (Hopkins, 1986). These fish have three types of electroreceptors in their skin: mormyromasts are used for active sensing, ampullary receptors for passive sensing and knollenorgans for commun...