Lon A. Wilkens

Use of behavioural stochastic resonance by paddle fish for feeding.

Stochastic resonance is the phenomenon whereby the addition of an optimal level of noise to a weak information-carrying input to certain nonlinear systems can enhance the information content at their outputs. Computer analysis of spike trains has been needed to reveal stochastic resonance in the responses of sensory receptors except for one study on human psychophysics. But is an animal aware of, and can it make use of, the enhanced sensory information from stochastic resonance? Here, we show that stochastic resonance enhances the normal feeding behaviour of paddlefish (Polyodon spathula), which use passive electroreceptors to detect electrical signals from planktonic prey. We demonstrate significant broadening of the spatial range for the detection of plankton when a noisy electric field of optimal amplitude is applied in the water. We also show that swarms of Daphnia plankton are a natural source of electrical noise. Our demonstration of stochastic resonance at the level of a vital animal behaviour, feeding, which has probably evolved for functional success, provides evidence that stochastic resonance in sensory nervous systems is an evolutionary adaptation.

Low-Dimensional Dynamics in Sensory Biology 1: Thermally Sensitive Electroreceptors of the Catfish

We report the results of a search for evidence of periodic unstableorbits in the electroreceptors of the catfish. The function of thesereceptor organs is to sense weak external electric fields. Inaddition, they respond to the ambient temperature and to the ioniccomposition of the water. These quantities are encoded by receptorsthat make use of an internal oscillator operating at the level of themembrane potential. If such oscillators have three or more degreesof freedom, and at least one of which also exhibits a nonlinearity,they are potentially capable of chaotic dynamics. By detecting theexistence of stable and unstable periodic orbits, we demonstratebifurcations between noisy stable and chaotic behavior using theambient temperature as a parameter. We suggest that the techniquedeveloped herein be regarded as an additional tool for the analysisof data in sensory biology and thus can be potentially useful instudies of functional responses to external stimuli. We speculatethat the appearance of unstable orbits may be indicative of a stateof heightened sensory awareness by the animal.

THE PADDLEFISH ROSTRUM FUNCTIONS AS AN ELECTROSENSORY ANTENNA IN PLANKTON FEEDING

A novel electrosensory function is presented for the large, plankton–feeding, freshwater paddlefish, Polyodon spathula, along with a hypothesis which accounts for the distinctive, elongated rostrum of this unusual fish. Behavioural experiments conducted in the ‘dark’ (under infrared illumination), to eliminate vision, show that paddlefish efficiently capture planktonic prey to distances up to 80–90 mm. They make feeding strikes at dipole electrodes in response to weak low–frequency electrical currents. Fish also avoid metal obstacles placed in the water, again in the dark. Electrophysiological experiments confirm that the Lorenzinian ampullae of paddlefish are sensitive to weak, low–frequency electrical signals, and demonstrate unequivocally that they respond to the very small electrical signals generated by their natural zooplankton prey (Daphnia sp.). We propose that the rostrum constitutes the biological equivalent of an electrical antenna, enabling the fish to accurately detect and capture its planktonic food in turbid river environments where vision is severely limited. The electrical sensitivity of paddlefish to metallic substrates may interfere with their migrations through locks and dams.

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.

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. J. Comp. Neurol. 446:25–36, 2002.

The Paddlefish Rostrum as an Electrosensory Organ: A Novel Adaptation for Plankton Feeding

ABSTRACT The ancient Mississippi River paddlefish, Polyodon spathula, has long been thought to use its oversized rostrum for excavation. Recent studies provide an entirely new interpretation for the function of the paddle, that of an electrical antenna for detecting the electric fields of plankton, P. spathulas primary food. Feeding experiments with juvenile fish demonstrate that paddlefish detect and capture individual daphnia when all sensory modalities except the electrosense have been blocked. The paddle provides space for an extravagant array of ampullary electroreceptors that are found in common with elasmobranchs and primitive bony fish. This exquisite electrosensory organ may also influence the migration of paddlefish in an environment replete with dams and other steel structures, sources of unnatural electric signals (corrosion potentials). In the laboratory, paddlefish are sensitive to and avoid metallic obstacles, even in the dark. Electrosensory processing in the brain involves physiological mechanisms for spatial imaging equivalent to planktivory based on passive electrosensitivity.

TEMPERATURE DEPENDENCE AND THE ROLE OF INTERNAL NOISE IN SIGNAL TRANSDUCTION EFFICIENCY OF CRAYFISH MECHANORECEPTORS

A simple phenomenon called stochastic resonance (SR), well known in nonlinear statistical physics, offers an explanation of how random fluctuations can enhance the detectability and/or the coherence of a weak signal in certain nonlinear dynamical systems. It is interesting to speculate that SR may play a role in the remarkable sensitivity exhibited by numerous biological sensory systems: systems which are themselves often inherently noisy and which, moreover, must usually operate in a noisy environment. A distinction is thus drawn between the external, or environmental, noise and the internal noise inherent in the sensory neurons themselves and distinguished by the randomness in time intervals between action potential spikes. We report the results of experiments with the internal noise, the intensity of which is varied by controlling the temperature of the preparation during the experiment. The useful range of temperatures could be extended by acclimating individual crayfish to a low or high temperature environment for many weeks prior to the experiment. Our results indicate that noise plays a significant role in signal transduction efficiency, increasing the signal-to-noise (SNR) ratio exponentially with noise intensity up to a maximum. Increasing the temperature beyond this maximum results in reduced SNRs and sharply reduced internal noise levels. The results of shifts in the data due to acclimation temperature can be removed by plotting the data versus the noise level, indicating that the noise may be a universal quantity in the dynamics of biological neurons.

Neurobiology of the scallop. II: Structure of the parietovisceral ganglion lateral lobes in relation to afferent projections from the mantle eyes

The lateral lobes of the scallop parietovisceral ganglion have been examined morphologically with respect to their functional role as optic lobes. The gross morphology of the lateral lobe and projections of optic nerve fibers within it were investigated by 1) supravital methylene blue staining, and 2) autoradiography using tritiated proline injected intraocularly for incorporation and transport by the optic fibers. Ultrastruc‐turally, the lateral lobe was examined using standard electron microscopic techniques. The lateral lobe is composed of a cortical rind of cells, 8–15 μm in diameter at the ventral surface and 15–20 μm in diameter at the ventral surface, surrounding a central neuropil. The neuropil contains three distinct regions: 1) the glomerular neuropil, a series of densely staining spherical subunits associated with the eyes and pallial nerves, 2) the subcellular neuropil, a synaptic region adjacent to the ventral cell layer also having a visual function, and 3) the subglomerular neuropil, the re...

Primary afferent electrosensory neurons represent paddlefish natural prey

Abstract The paddlefish detects electric fields of its planktonic prey. Each plankton particle, such as a moving Daphnia , is an electric dipole. Primary afferent neurons of the paddlefish electrosensory system were found to respond transiently to moving dipoles (i.e., Daphnia ) within their receptive field. Positive plankton potential increases and negative potential decreases the primary afferent spike rate while biphasic plankton potentials elicit biphasic neuronal responses. That is to say, neuronal activity coincides with the planktons electric dipole potentials. Consequently, responses of primary afferent neurons could have ambiguous effects on second-order pyramidal-like neurons: an increase of firing rate should depolarize and a decrease of firing rate should hyperpolarize the postsynaptic membrane potential of second-order neurons. Depending on its orientation, a plankton particle passing the receptive field would elicit opposite central effects. Nevertheless, because paddlefish feed successfully on plankton particles, the central nervous system must process primary afferent signals so as to unambiguously represent the position of a plankton particle.

Stochastic synchronization of electroreceptors in paddlefish

We studied synchronization of electrosensitive cells of the paddlefish by means of electrophysiological experiments. We found that primary afferents of the paddlefish are represented by noisy nonlinear oscillators. Different types of phase locked regimes are observed. The influence of internal noise is discussed.