The electrosense is a specialized sensory modality of ancient fish and is best known in sharks that are able to detect the electrical fields of potential prey at close range and to use electromagnetic fields for navigation. Whereas these are macroscopic functions of the electrosense, the electrosensory system in the freshwater paddlefish has recently been shown to detect the weak electric fields of tiny plankton, the primary food source for the fish. The electroreceptors of this novel sensory system are present on an elongated rostrum, one-third the length of the fish, which constitutes an electrosensory organ the equivalent of an antenna. The exquisite sensitivity of this organ and its behavioral role in targeting planktonic prey makes it a useful model preparation in which to investigate the sensory processing of spatial features in the environment. Importantly, the brain contains a large, easily distinguishable region that is well suited for exploring the neural processing that underlies the feeding behavior. Dr. Wilkens' objective in this research proposal is to elucidate the neural circuitry and algorithms that enable the paddlefish to selectively target single plankton adrift in the turbid water column. Dr. Wilkens will study the electric signaling properties of sensory fibers coming from the receptors on the rostrum and the properties of neurons that the fibers contact in the hindbrain region, the dorsal octavolateralis nucleus (DON), which first processes the electrosensory information. Initial experiments will investigate the organization of sensory input into the DON. In sensory systems from other animals there is typically a topographic representation of peripheral receptive fields mapped out onto their target cells in the brain, such that adjacent brain cells correspond to nearby receptive fields. Early physiological recordings, however, have found no evidence for such topography in the paddlefish brain. To further investigate this unusual feature, Dr. Wilkens will use histological staining techniques that trace the nerve projections of the sensory fibers into the brain. This will provide direct neuroanatomical evidence for the organization of electrosensory processing in the brain. If it is confirmed that there is no topographical organization, other mechanisms for extracting spatial features must exist. Previous records of neural impulse activity from nerve cells in the DON show that their firing rates reflect the first derivative of an electrosensory stimulus waveform. Thus, brain cells respond preferentially to dynamical features of the stimulus signal, rather than to its magnitude. With the possibility that anatomical data will confirm the absence of spatial topography in the DON, Dr. Wilkens has developed a computer simulation model of a derivative filter whereby the information about the distance and velocity of an environmental signal could be encoded in the response neurons of the DON. The model will be tested by presenting electrical stimuli that move over the receptive fields in the rostrum, thus simulating the planktonic electric fields encountered by the fish during normal swimming. Recordings from these cells will be followed by the injection of nerve stains to trace their projections into higher midbrain regions. It is hypothesized that topographic representation will be established in the terminal projections of DON cells in the midbrain. Dr. Wilkens' descriptions of the electrosense in paddlefish has had broad implications for fisheries management of this threatened species, providing an explanation for why fish avoid metal structures (dams) in the rivers in addition to becoming an important model system for studying brain function. Dr. Wilkens will actively recruit underrepresented students from the St. Louis urban region to participate in this project.
