Dynamic changes in level influence spatial coding in the lateral superior olive

Abstract

It is well established that the responses of binaural auditory neurons can adapt and change dramatically depending on the nature of a preceding sound. Examples of how the effects of ensuing stimuli play a functional role in auditory processing include motion sensitivity and precedence-like effects. To date, these types of effects have been documented at the level of the midbrain and above. Little is known about sensitivity to ensuing stimuli below in the superior olivary nuclei where binaural response properties are first established. Here we report on single cell responses in the gerbil lateral superior olive, the initial site where sensitivity to interaural level differences is established. In contrast to our expectations we found a robust sensitivity to ensuing stimuli. The majority of the cells we tested (86%), showed substantial suppression and/or enhancement to a designated target stimulus, depending on the nature of a preceding stimulus. Hence, sensitivity to ensuing stimuli is already established at the first synaptic station of binaural processing.

Figure 1

Effects of preceding stimuli on the responses to a standard target stimulus for an example LSO neuron. A. Preceding and target stimuli were ILDs selected from the dynamic portion of the neuron’s ILD function. ILD functions were generated with 250 ms tones presented at the neuron’s best frequency. For this neuron, the intensity to the ipsilateral, excitatory ear was held fixed at 40 db, SPL and the intensity to the contralateral, inhibitory ear was varied from 20–70 dB, SPL. The curve shows that spike number decreased as a function of increasing contralateral intensity. B–D Raster plots showing spike activity during presentation of a preceding stimulus and a following target stimulus (50 presentations). The ILD of the target stimulus is the same as the ILD indicated by the grey arrow in A. B shows responses for a preceding stimulus with a less intense signal to the inhibitory ear (corresponding to the ILD indicated by the black arrow in A). C shows the responses for a preceding stimulus that was the same as the target. D shows responses for a preceding stimulus with a more intense signal to the inhibitory ear (corresponding to the ILD indicated by the open arrow in A). E–G Peri-stimulus time histograms corresponding to the raster plots (spikes binned into 20 ms bins). The first three bars corresponds to the last 60 ms with the preceding stimulus. The remaining 12 bins correspond to the first 240 ms with the target. In each of the tree histograms, the grey bars show spike-counts for the target stimulus when it was preceded by itself. The open bars show spike-counts for the target when it was preceded by an ILD with a less intense signal to the inhibitory ear (E) or an ILD with a more intense signal to the inhibitory ear (G).

Figure 2

Peri-stimulus time histograms for three neurons (A–C) tested with preceding stimuli as described in Figure 1. See text for detail.

Figure 3

Magnitude of effects for the 37 neurons tested. A. Suppression values along the x-axis correspond to the percentage decrease in spike-count for the target stimulus preceded by an ILD with a less intense signal to the inhibitory ear. Enhancement values along the y-axis correspond to the percentage increase in spike-count for the target stimulus preceded by an ILD with a more intense signal to the inhibitory ear. The regression line and correlation coefficient indicate no correlation between magnitude of suppression and enhancement. B. The combination of the percentage increase corresponding to enhancement and the percentage decrease corresponding to suppression is plotted for each neuron as an index of overall effects of preceding stimuli. The values are in rank order of effect size.

Figure 4

Effects from preceding stimuli are lost with a relatively long inter-stimulus-interval but not with a relatively long stimulus duration. A. The percentage difference between suppression and enhancement for seven neurons tested with the standard 0 ms inter-stimulus-interval (circles) and a relatively long inter-stimulus-interval of 2,750 ms (triangles). B. The percentage difference between suppression and enhancement for five neurons tested with the standard stimulus duration of 250 ms (circles) and a relatively long stimulus duration of 3,000 ms (triangles). Each neuron shows substantial effects for both durations.

Figure 5

Effects of changing excitation versus inhibition in generating the preceding stimulus. A. Peri-stimulus time histograms from a neuron tested with the standard stimulus paradigm where the intensity to the inhibitory signal was manipulated. B. Peri-stimulus time histograms from the same neuron when the intensity of the excitatory signal was manipulated. Both stimulus paradigms induce suppression and enhancement. C. The percentage difference between suppression and enhancement for ten neurons tested with both stimulus paradigms.

Figure 6

Effects of stimulating only the excitatory ear. A. Peri-stimulus time histograms from a neuron tested with monaural, excitatory stimuli. This neuron showed suppression to the monaural target when it was preceded by a more intense monaural stimulus (top) and enhancement when the target was preceded by a less intense monaural stimulus (bottom). B. The percentage difference between suppression and enhancement for five neurons tested with monaural stimuli.