Receptive field organization of electrosensory neurons in the paddlefish (Polyodon spathula).

Paddlefish use their electrosense to locate small water fleas (daphnia), their primary prey, in three-dimensional space. High sensitivity and a representation of object location are essential for this task. High sensitivity can be achieved by convergence of information from a large number of receptors and object location is usually represented in the nervous system by topographic maps. However the first electrosensory center in the brain, the dorsal octavolateral nucleus in the hindbrain, is neither topographically organized nor does it show a higher sensitivity than primary afferent fibers. Here, we investigated the response properties of electrosensory neurons in the dorsal octavolateral nucleus (DON), the lateral mesencephalic nucleus (LMN) and the tectum mesencephali (TM). LMN units are characterized by large receptive fields, which suggest a high degree of convergence. TM units have small receptive fields and are topographically arranged, at least in the rostro-caudal axis, the only dimension we could test. Well-defined receptive fields, however, could only be detected in the TM with a moving DC stimulus. The receptive fields of TM units, as determined by slowly scanning the rostrum and head with a 5 Hz stimulus, were very large and frequently two or more receptive fields were present. The receptive fields for LMN units were located in the anterior half of the rostrum whereas TM units had receptive fields predominantly on the head and at the base of the rostrum. A detailed analysis of the prey catching behavior revealed that it consists of two phases that coincide with the location of the receptive fields in LMN and TM, respectively. This suggests that LMN units are responsible for the initial orienting response that occurs when the prey is alongside the anterior first half of the rostrum. TM units, in contrast, had receptive fields at locations where the prey is located when the fish opens its mouth and attempts the final strike.

Response properties of electrosensory units in the midbrain tectum of the paddlefish (Polyodon spathula Walbaum).

Paddlefish use their peculiar rostrum to detect minute electric fields from their main prey, small water fleas. Electroreceptors over the rostrum and head sense these fields and send the information into a single hindbrain area, the dorsal octavolateral nucleus (DON). From there, information is sent to various midbrain structures, including the tectum. The response properties of primary afferent fibers and DON units has been well investigated, but nothing is known about electrosensory units in the midbrain. Here we recorded the responses of single units in the midbrain tectum and DON to uniform electric fields. Tectal units exhibited little spontaneous activity and responded to sine waves with a few, well phase-locked spikes. Phase locking was still significant at amplitudes one order of magnitude lower than in the DON. If stimulated with sinusoidal electric fields of different frequencies, phase locking in DON units decreased proportionally with frequency whereas the response of tectal units depended little on frequency. This is in agreement with behavioral studies showing that relevant frequencies range from DC to ca 20 Hz.