Two modes of information processing in the electrosensory system of the paddlefish (Polyodon spathula).

Paddlefish are uniquely adapted for the detection of their prey, small water fleas, by primarily using their passive electrosensory system. In a recent anatomical study, we found two populations of secondary neurons in the electrosensory hind brain area (dorsal octavolateral nucleus, DON). Cells in the anterior DON project to the contralateral tectum, whereas cells in the posterior DON project bilaterally to the torus semicircularis and lateral mesencephalic nucleus. In this study, we investigated the properties of both populations and found that they form two physiologically different populations. Cells in the posterior DON are about one order of magnitude more sensitive and respond better to stimuli with lower frequency content than anterior cells. The posterior cells are, therefore, better suited to detect distant prey represented by low-amplitude signals at the receptors, along with a lower frequency spectrum, whereas cells in the anterior DON may only be able to sense nearby prey. This suggests the existence of two distinct channels for electrosensory information processing: one for proximal signals via the anterior DON and one for distant stimuli via the posterior DON with the sensory input fed into the appropriate ascending channels based on the relative sensitivity of both cell populations.

Nonlinear dynamics of skin potentials in the electrosensory paddlefish.

It is known that steady skin potentials are present in fishes due to chloride pumps in the gills and in the skin. We have found previously that these skin potentials can fluctuate and oscillate in the electrosensory paddlefish. Here we show that larger, discharge like potentials can be triggered by applying external electric fields in the water surrounding the fish. These resemble action potentials in nerve cells, but have a longer time scale. Like action potentials, these discharges travel laterally in the skin. They start at the tip of the rostrum and propagate caudally to the tip of the gill covers. They follow the all-or-nothing rule and need some refractory period before they can be evoked again. This is the first time that such discharges, so strikingly similar to action potentials, have been described at the level of a whole organism.

Descending projections to the hindbrain and spinal cord in the paddlefish Polyodon spathula.

In vertebrates, almost all motor neurons innervating skeletal muscles are located in the hindbrain and spinal cord, and all brain centers that control behavior have descending projections into these parts of the central nervous system. With tracer injections into the spinal cord and hindbrain, we have studied cell groups with descending projections in the paddlefish. Spinal cord injections reveal retrogradely labeled cells in all reticular and raphe nuclei, as well as the nucleus of the medial longitudinal fascicle. Additional cell groups with projections to the spinal cord are the nucleus of the fasciculus solitarius, descending trigeminal nucleus, several octavolateral nuclei, the dorsal hypothalamic nucleus, and the pretectum. The only primary sensory fibers with descending projections are trigeminal fibers. Hindbrain injections reveal a number of additional cell groups in di- and mesencephalon. The most prominent source is the mesencephalic tectum. Other descending cells were found in the dorsal posterior thalamic nucleus, ventral thalamus, torus semicircularis, lateral mesencephalic nucleus, and the central gray of the mesencephalon. Our data show that descending spinal projections are comparable to those of other vertebrates and that the tectum is the most important motor control center projecting to the hindbrain. A surprising result was that the dorsal posterior thalamic nucleus also projects to the hindbrain. This nucleus is thought to be a center that relays sensory information to the telencephalon. Further studies are needed to determine the complete set of projections of the dorsal thalamus in paddlefish and other fishes to gain insights into its functional role.

Edge-detection filter improves spatial resolution in the electrosensory system of the paddlefish.

In many fishes, prey capture is guided primarily by vision. In the paddlefish, the electrosense can completely substitute for the visual system to detect tiny daphnia, their primary prey. Electroreceptors are distributed over the entire rostrum, head, and gill covers, and there are no accessory structures like a lens to form an image. To accurately locate planktonic prey in three-dimensional space, the poor spatial resolving power of peripheral receptors has to be improved by another mechanism. We have investigated information processing in the electrosensory system of the paddlefish at hind- and midbrain levels by recording single cells extracellularly. We stimulated with a linear array of electrodes that simulated a moving dipole field. In addition, global electric fields were applied to simulate the temporal component of a moving dipole only. Some stimulation were done with sinusoidal fields. The fire rate of cells in the hindbrain followed the first derivative of the stimulus wave form. In contrast, the response of tectal cells were similar to the third derivative. This improves spatial resolution and receptive fields of tectal units are much smaller than the ones of hind brain units. The principle is similar to a Laplacian of Gaussian filter that is commonly used in digital image processing. However, instead of working in the space domain, the paddlefish edge detection filter works in the time domain, thus eliminating the need for extensive interconnections in an array of topographically organized neurons.

Two parallel ascending pathways from the dorsal octavolateral nucleus to the midbrain in the paddlefish Polyodon spathula.

The paddlefish is a passive electrosensory ray-finned fish with a special rostral appendage that is covered with thousands of electroreceptors, which makes the fish extremely sensitive to electric fields produced by its primary prey, small water fleas. We reexamined the electrosensory pathways from the periphery to the midbrain by injecting the neuronal tracer BDA into different branches of the lateral line nerve and into different parts of the dorsal octavolateral nucleus (DON) and the tectum. Primary afferents from the anterior to posterior body axis terminate in different areas in the mediolateral axis of the DON, the first electrosensory processing station. Previous studies showed that DON neurons project to the tectum and two different areas in the tegmentum. Now, we have found differences between the anterior and the posterior DON. Fibers from the anterior DON project unilaterally to the contralateral tectum while its posterior neurons project bilaterally to two nuclei in the tegmentum, the torus semicircularis and the lateral mesencephalic nucleus. This study is the first to show that two different populations of ascending neurons project to two different targets in the midbrain. These two pathways are likely to have different functions and further investigations may reveal the functional significance of these two parallel ascending systems.

Response properties of electrosensory neurons in the lateral mesencephalic nucleus of the paddlefish.

Many fishes and amphibians are able to sense weak electric fields from prey animals or other sources. The response properties of primary afferent fibers innervating the electroreceptors and information processing at the level of the hindbrain is well investigated in a number of taxa. However, there are only a few studies in higher brain areas. We recorded from electrosensory neurons in the lateral mesencephalic nucleus (LMN) and from neurons in the dorsal octavolateral nucleus (DON) of the paddlefish. We stimulated with sine wave stimuli of different amplitudes and frequencies and with moving DC stimuli. During sinusoidal stimulation, DON units increased their firing rate during the negative cycle of the sine wave and decreased their firing rate to the positive cycle. Lateral mesencephalic nucleus units increased their rate for both half cycles of the sine wave. Lateral mesencephalic nucleus units are more sensitive than DON units, especially to small moving dipoles. Dorsal octavolateral nucleus units respond to a moving DC dipole with an increase followed by a decrease in spike rate or vice versa, depending on movement direction and dipole orientation. Lateral mesencephalic nucleus units, in contrast, increased their discharge rate for all stimuli. Any change in discharge rate of DON units is converted in the LMN to a discharge rate increase. Lateral mesencephalic nucleus units therefore appear to code the presence of a stimulus regardless of orientation and motion direction.

Resonant properties in the paddlefish electrosensory system caused by delayed feedback.

INTRODUCTION: The paddlefish electrosensory system consists of receptor cells in the skin that sense minute electric fields from their prey, small water fleas. The receptors thereby measure the difference of the voltage at the skin surface against the voltage inside the animal. Due to a high skin impedance, this internal voltage is considered to be relatively fixed. RESULTS: We found, however, that this internal voltage can fluctuate. It shows damped oscillations to a single short electric field pulse and changes, with some time delay, according to the previous history of stimulation, and shows resonance at a certain frequency. CONCLUSIONS: Computer simulations show that these phenomena can be explained by the presence of delayed feedback where the internal voltage is part of the feedback loop.

Response properties of electrosensory afferent fibers and secondary brain stem neurons in the paddlefish.

The passive electrosense is used by many aquatic animals to detect weak electric fields from other animals or from geoelectric sources. In contrast to the active electrosense, ;passive' means that there are no electric organs, and only external fields are measured. Electroreceptors are distributed in the skin, but are different from other skin senses because they can detect and localize sources a considerable distance away. Distant sources, however, stimulate a large number of receptors at the same time and central circuits have to compute the exact location of the source from this distributed information. In order to gain insights into the algorithms involved, we compared the response properties of units in the dorsal octavolateral nucleus (DON) with primary afferent fibers in the paddlefish. The following parameters were tested: spontaneous activity, sensitivity, frequency tuning, receptive field size, movement sensitivity, and topography within the DON. Although there are some differences in spontaneous activity and receptive field size, there are no major differences between primary afferents and DON units that could reveal any substantial amount of spatial information processing. In particular the lack of any topographic order within the DON renders a lateral interaction between neighboring receptive fields unlikely.

Temporal analysis of moving DC electric fields in aquatic media.

Many aquatic vertebrates can sense the weak electric fields generated by other animals and may also sense geoelectric or electromagnetic phenomena for use in orientation. All these sources generate stationary (dc) fields. In addition, fields from animals are modulated by respiration and other body movements. Since electroreceptors are insensitive to a pure dc field, it has been suggested that the ac modulation carries most of the relevant information for electrosensory animals. However, in a natural situation pure dc fields are rare since any relative movement between source and receiver will transform a dc field into a time varying signal. In this paper, we will describe the properties of such signals and how they are filtered at the first stage of electrosensory information processing in the brain. We will show that the signal perceived by an animal traversing a dc electric field contains all the information necessary to reconstruct the distance to the source and that the signal conditioning algorithms are perfectly adapted to preserve such information.

Phase synchronization and stochastic resonance effects in the crayfish caudal photoreceptor.

We study the nonlinear response of the crayfish caudal photoreceptor to periodic mechanical stimuli in terms of stochastic synchronization. The amplitude and frequency of the mechanical stimuli and the light level are used as control parameters. The system shows multiple locking regions as the stimulus frequency is varied. We find that the synchronization index increases as the signal-to-noise ratio (SNR) of the periodic drive, in response to increasing light levels; this effect exhibits features similar to stochastic resonance. We demonstrate a nonlinear rectification effect in which the SNR of the second harmonic of the input stimulus increases as the light level is raised, and show that the corresponding synchronization index increases as the SNR of the second harmonic.

Central organization of the electrosensory system in the paddlefish (Polyodon spathula).

The central connections of the electrosensory system were studied in the paddlefish Polyodon spathula by injecting biotinylated dextran amines into the dorsal octavolateral nucleus (DON), the cerebellum, and the mesencephalic tectum. The sole target of primary electrosensory fibers is the ipsilateral dorsal octavolateral nucleus. The principal neurons ascending from this nucleus project to the torus semicircularis, the lateral mesencephalic nucleus, and the mesencephalic tectum. The mesencephalic tectum projects back to the nucleus preeminentialis, which, in turn, projects to the cerebellar auricles and to the DON. The auricles are the main source of parallel fibers in the cerebellar crest ventral to the DON. The DON also receives input from the contralateral DON. These descending feedback loops are very similar to those of other electrosensory fishes. However, the paddlefish is unique in having three mesencephalic targets of electrosensory information. It is the only bony fish known to have extensive projections directly to the mesencephalic tectum and to a lateral mesencephalic nucleus in addition to the torus semicircularis.

The electric sense of the paddlefish: a passive system for the detection and capture of zooplankton prey.

Behavioral and electrophysiological experiments have shown that the elongated paddlefish rostrum, with its extensive population of ampullae of Lorenzini, constitutes a passive electrosensory antenna of great sensitivity and spatial resolution. As demonstrated in juvenile paddlefish, the passive electrosense serves a novel function in feeding serving as the primary, if not exclusive sensory modality for the detection and capture of zooplanktonic prey. Ampullary receptors are sensitive to the weak electrical fields of plankton from distances up to 9 cm, and juvenile paddlefish capture plankton individually with great swimming dexterity in the absence of vision or other stimulus signals. Paddlefish also detect and avoid metal obstacles, the electrical signatures of which are a potential hindrance to their feeding and reproductive migrations. The ampullary receptors, their peripheral innervation and central targets in the dorsal octavolateral nucleus, are described. We also describe the ascending and descending neuronal circuitry of the electrosensory system in the brain based on tracer studies using dextran amines.