The Journal of Neuroscience, September 1, 1999, 19(17):7629-7639

Frequency-Dependent PSP Depression Contributes to Low-Pass Temporal Filtering in Eigenmannia

Department of Biology, University of Utah, Salt Lake City, Utah 84112-0840

This study examined the contribution of frequency-dependent short-term depression of PSP amplitude to low-pass temporal filtering in the weakly electric fish Eigenmannia. Behavioral and neurophysiological methods were used. Decelerations of the electric organ discharge frequency were measured in response to continuous and discontinuous electrosensory stimuli. Decelerations were strongest (median = 4.7 Hz; range, 3.5-5.9 Hz) at continuous beat rates of ~5 Hz and weakest (median = 0.4 Hz; range, 0.0-0.8 Hz) at beat rates of 30 Hz. Gating 20 or 30 Hz stimuli at a rate of 5 Hz, however, elicited decelerations that were sixfold greater than that of continuous stimuli at these beat rates (median = 2.6 Hz; range, 2.0-4.7 Hz for 30 Hz). These results support the hypothesis that short-term processes enhance low-pass filtering by reducing responses to fast beat rates. This hypothesis was tested by recording intracellularly the responses of 33 midbrain neurons to continuous and discontinuous stimuli. Results indicate that short-term depression of PSP amplitude primarily accounts for the steady-state low-pass filtering of these neurons beyond that contributed by their passive and active membrane properties. Previous results demonstrate that passive properties can contribute up to 7 dB of low-pass filtering; PSP depression can add up to an additional 12.5 dB (median = 4.5). PSP depression increased in magnitude with stimulus frequency and showed a prominent short-term component (t₁ = 66 msec at 30 Hz). Initial PSP amplitude recovered fully after a gap of 150 msec for most neurons. Remarkably, recovery of PSP amplitude could be produced by inserting a brief low-temporal frequency component in the stimulus.

Key words: whole-cell patch; sensory processing; adaptation; torus semicircularis; jamming avoidance response; synaptic depression; plasticity