TEMPORAL FILTERING PROPERTIES OF AMPULLARY ELECTROSENSORY NEURONS IN THE TORUS-SEMICIRCULARIS OF EIGENMANNIA - EVOLUTIONARY AND COMPUTATIONAL IMPLICATIONS

Weakly electric fish have parallel electrosensory systems, the phyloge netically older ampullary system and the novel tuberous system. The tu berous systems an adaptation related to the evolution of active electr olocation. To examine the evolutionary relationship of the ampullary a nd tuberous systems, the temporal filtering properties of ampullary ne urons in the dorsal torus semicircularis of Eigenmannia were studied. 'Whole-cell' recordings were made in vivo using patch-type pipettes. T he responses of 19 neurons to sinusoidal electric signals (<40 Hz) wer e recorded and the anatomy of these neurons demonstrated by injection of biocytin. All eight low-pass ampullary neurons had broad, relativel y smooth post-synaptic potentials (psps) that at low frequencies nicel y reflected the sinusoidal stimuli. These neurons had somata of 10-14 mu m diameter and thick, spiny dendrites. Eight high-pass neurons were recorded, representing three physiological classes. The first class ( 3 neurons) had psps that roughly followed the sinusoidal time course o f the stimulus; the psp morphology was similar to low-pass neurons. Th e second class had many small, fast, individual psps; their rate of oc currence varied with the stimulus. Finally, four neurons showed psps t hat were of constant width across stimulus frequencies. All three clas ses of high-pass neurons had small somata (8-10 mu m diameter) with th in dendrites and. either few or no spines. Some of these neurons had l arge varicosities on the dendrites. Three neurons had band-pass filter ing properties: neurons that showed strong band-pass properties were m orphologically similar to low-pass neurons. Comparisons of the tempora l filtering, shapes of post-synaptic potentials, and anatomy of ampull ary and tuberous neurons in the torus suggest that the circuitry for t uberous processing in the torus may have evolved as an elaboration or duplication of the ampullary system. The mechanisms underlying the low -pass filtering characteristics of tuberous neurons therefore appear t o have predated the evolution of the tuberous system and to have serve d as a pre-adaptation for the evolution of the jamming avoidance respo nse. In addition, these data support the hypothesis that spine density influences the temporal filtering properties of neurons.