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In one species of vocalizing (sonic) fish, the midshipman (Porichthys notatus), there are two classes of sexually mature males--Types I and II--distinguished by a number of traits including body size, gonad size, and reproductive tactic. The larger Type-I males (unlike Type-II males and females) build nests, guard eggs, and generate several types of vocalizations. Sound production by Type-I males is paralleled by a proportionate increase of 600% in their sonic muscle mass. The motor volley from ventral occipital roots innervating the sonic muscles establishes their contraction rate and, in turn, the fundamental frequency of emitted sounds. Electrical stimulation of the midbrain in every male and female elicited a rhythmic sonic discharge as recorded in the occipital roots; however, the fundamental frequency was slightly, but significantly, higher (20%) in Type-I males. Intracellular recording from identified motoneurons and presumed presynaptic "pacemaker" neurons showed their synaptic and action potentials had the same frequency as that of the nerve volley in every male and female. Reconstructions of physiologically identified motoneurons and pacemaker neurons following intracellular horseradish-peroxidase (HRP) filling showed their somata and dendrites to be 100-300% larger in Type-I males. These data unambiguously show that the size of a target muscle is correlated with the size of both the respective motoneurons and their presynaptic afferent neurons. As discussed, this implies that the dramatic increase in neuron size in the sonic motor system of Type-I males is causally dependent upon expansion of the sonic muscle. It is further likely that the more modest sex difference in the rhythmic central discharge is established by the intrinsic membrane properties of sonic neurons. These results also corroborate, at a number of behavioral, morphological, and neurophysiological levels, that the sonic motor system of "sneak spawning" Type-II males is similar to that of females. Thus, unlike the vocalizing Type-I males, sexual differentiation of the reproductive system in Type-II males is not linked to concomitant changes in the neurophysiological and morphological features of the sonic motor circuit.

Baker. Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 92: 3546 -3561, 2004. First published July 21, 2004 doi:10.1152/ jn.00311.2004. We quantitatively studied the ontogeny of oculomotor behavior in larval fish as a foundation for studies linking oculomotor structure and function with genetics. Horizontal optokinetic and vestibuloocular reflexes (OKR and VOR, respectively) were measured in three different species (goldfish, zebrafish, and medaka) during the first month after hatching. For all sizes of medaka, and most zebrafish, Bode plots of OKR (0.065-3.0 Hz, Ϯ10°/s) revealed that eye velocity closely followed stimulus velocity (gain Ͼ 0.8) at low frequency but dropped sharply above 1 Hz (gain Ͻ 0.3 at 3 Hz). Goldfish showed increased gain proportional to size across frequencies. Linearity testing with steps and sinusoids showed excellent visual performance (gain Ͼ 0.8) in medaka almost from hatching; but zebrafish and goldfish exhibited progressive improvement, with only the largest equaling medaka performance. Monocular visual stimulation in zebrafish and goldfish produced gains of 0.5 versus Ͻ0.1 for the eye viewing a moving versus stationary stimulus pattern but 0.25 versus Ͻ0.1 in medaka. Angular VOR appeared much later than OKR, initially at only high accelerations (Ͼ200°/s at 0.5 Hz), first in medaka followed by larger (8.11 mm) zebrafish; but it was virtually nonexistent in goldfish. Velocity storage was not observed except for an eye velocity build-up in the largest medaka. In summary, a robust OKR was achieved shortly after hatching in all three species. In contrast, larval fish seem to be unique among vertebrates tested in their lack of significant angular VOR at stages where active movement is required for feeding and survival.

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Summary Background Whilst adult vertebrates sense changes in head position using two classes of accelerometer, at larval stages zebrafish lack functional semicircular canals and rely exclusively on their otolithic organs to transduce vestibular information. Results Despite this limitation, we find that larval zebrafish perform an effective vestibulo-ocular reflex (VOR) that serves to stabilize gaze in response to pitch and roll tilts. Using single-cell electroporations and targeted laser-ablations, we identified a specific class of central vestibular neurons, located in the tangential nucleus, which are essential for the utricle-dependent VOR. Tangential nucleus neurons project contralaterally to extraocular motoneurons, and in addition, to multiple sites within the reticulospinal complex. Conclusion We propose that tangential neurons function as a broadband inertial accelerometer, processing utricular acceleration signals to control the activity of extraocular and postural neurons, thus completing a fundamental three-neuron circuit responsible for gaze stabilization.

In neural integrators, transient inputs are accumulated into persistent firing rates that are a neural correlate of short-term memory. Integrators often contain two opposing cell populations that increase and decrease sustained firing as a stored parameter value rises. A leading hypothesis for the mechanism of persistence is positive feedback through mutual inhibition between these opposing populations. We tested predictions of this hypothesis in the goldfish oculomotor velocity-to-position integrator by measuring the eye position and firing rates of one population, while pharmacologically silencing the opposing one. In complementary experiments, we measured responses in a partially silenced single population. Contrary to predictions, induced drifts in neural firing were limited to half of the oculomotor range. We built network models with synaptic-input thresholds to demonstrate a new hypothesis suggested by these data: mutual inhibition between the populations does not provide positive feedback in support of integration, but rather coordinates persistent activity intrinsic to each population.Persistent neural activity refers to a sustained discharge of action potentials that long outlasts a briefly presented stimulus, thus representing a short-term memory of the external cue. In neural integrator circuits, populations of neurons exhibiting graded levels of persistent activity store an accumulation of the stimulus over time: that is, a temporal integral. Neural integrators have been characterized at many levels of the nervous system, from brainstem to cortex 1-3 .

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The macroevolutionary events leading to neural innovations for social communication, such as vocalization, are essentially unexplored. Many fish vocalize during female courtship and territorial defense, as do amphibians, birds, and mammals. Here, we map the neural circuitry for vocalization in larval fish and show that the vocal network develops in a segment-like region across the most caudal hindbrain and rostral spinal cord. Taxonomic analysis demonstrates a highly conserved pattern between fish and all major lineages of vocal tetrapods. We propose that the vocal basis for acoustic communication among vertebrates evolved from an ancestrally shared developmental compartment already present in the early fishes.Although the genetic basis for human speech receives much attention [e.g., (1,2)], the fundamental issue of the ancestral origins of neural networks for vocal signaling is essentially unexplored. Social, context-dependent acoustic communication occurs in most of the major vertebrate lineages, including fishes (Fig. 1A). Teleost fish, the most species-rich of all vertebrate groups (3), have a simple repertoire of vocalizations complemented by vocal and auditory pathways that are organized similarly to those of amphibians, reptiles, birds, and mammals (4). Batrachoidid fish (midshipman and toadfish), in particular, have an expansive vocal-acoustic network, including a rhythmically firing, pacemaker-motor neuron circuit that directly determines the contraction rate of vocal muscles attached to the swim bladder and, in turn, the temporal properties of calls (5,6) ( Fig. 1B and fig. S1; movies S1 to S3). Because batrachoidids also have readily studied larval stages (7), they were chosen to investigate the hypothesis that fish and terrestrial vertebrates share an ancestral origin of their vocal motor networks. Here, we show that the vocal systems of fishes and tetrapods develop very similarly in a segment-like region that forms a transitional compartment between the caudal hindbrain and rostral spinal cord.