Journal of Neuroscience, Vol 13, 1178-1189, Copyright © 1993 by Society for Neuroscience
Temporal filtering properties of midbrain neurons in an electric fish: implications for the function of dendritic spines
GJ Rose and SJ Call
Department of Biology, University of Utah, Salt Lake City 84112.
Electrosensory neurons in the torus semicircularis (midbrain) of the weakly
electric fish Eigenmannia vary considerably in their dendritic structure
and responses to modulations of the amplitude of electric organ discharges.
We investigated possible relations between these properties by recording
intracellularly and labeling individual neurons while modulating stimulus
amplitude over rates of approximately 2-20 Hz. Morphologically distinct
cell types generally differed in their responses to these stimuli. The
amplitude envelope of the stimulus was nicely reflected in fluctuations of
the membrane potential of heavily spined neurons. The amplitude of these
stimulus-related depolarizations decreased markedly as the stimulus
modulation rate was increased. For aspiny or sparsely spined neurons,
however, the amplitude of stimulus- related depolarizations either
increased or remained constant over this range of modulation rates. In
these cells, the amplitude envelope of the stimulus was not well
represented in the membrane potential. Instead, fast EPSPs were observed
that varied in number over time in accordance with the amplitude envelope
of the stimulus. Aspiny neurons in the tectum also coded the amplitude
envelope of stimuli with poor fidelity. The amplitude of stimulus-related
depolarizations, however, decreased as the rate of modulation of stimulus
amplitude was increased, consistent with the notion that tectal neurons
receive afferent input from the spiny toral neurons. Spiny neurons appear,
therefore, to act as low-pass filters of temporal information in sensory
signals. Aspiny cells, however, code high temporal frequencies. These data
support the hypothesis that dendritic spines contribute to the low-pass
filtering of inputs to neurons.