Impact of response duration on multisensory integration

Abstract

Multisensory neurons in the superior colliculus (SC) have been shown to have large receptive fields that are heterogeneous in nature. These neurons have the capacity to integrate their different sensory inputs, a process that has been shown to depend on the physical characteristics of the stimuli that are combined (i.e., spatial and temporal relationship and relative effectiveness). Recent work has highlighted the interdependence of these factors in driving multisensory integration, adding a layer of complexity to our understanding of multisensory processes. In the present study our goal was to add to this understanding by characterizing how stimulus location impacts the temporal dynamics of multisensory responses in cat SC neurons. The results illustrate that locations within the spatial receptive fields (SRFs) of these neurons can be divided into those showing short-duration responses and long-duration response profiles. Most importantly, discharge duration appears to be a good determinant of multisensory integration, such that short-duration responses are typically associated with a high magnitude of multisensory integration (i.e., superadditive responses) while long-duration responses are typically associated with low integrative capacity. These results further reinforce the complexity of the integrative features of SC neurons and show that the large SRFs of these neurons are characterized by vastly differing temporal dynamics, dynamics that strongly shape the integrative capacity of these neurons.

Fig. 1.

Representative example of a single neuron recorded from the intermediate or deep layers of the superior colliculus (SC) that shows short-duration discharges at 4 of the representative locations tested within its receptive field. In fact, all the locations tested within the spatial receptive field of this neuron displayed short discharge duration. The spatial receptive field of the neuron is shown by a shaded rounded rectangle, top. Letters represent the locations for which poststimulus time histograms are shown below and bar graphs quantify the firing rates at each of the 3 stimulus conditions; interactive index (ii) values are also depicted. For the location represented by A within the receptive field there is significant response depression (*P = 0.016) and ii = −55.36%. For the location represented by B ii = 83%, which is also statistically significant (*P = 0.004). For the location represented by C ii = 60.45%, which is statistically significant (*P = 0.02 as determined by Wilcoxon rank test). The location represented by D exhibits significant interaction as expressed by ii = 80.61% (*P = 0.004). V, visual only; A, auditory only; VA, visual-auditory.

Fig. 2.

Representative example of a single neuron recorded from the intermediate or deep layers of the SC that shows a dual mode of discharge. Two of the representative locations show short response durations, while the rest show long response durations. The spatial receptive field of the neuron is shown by a shaded rounded rectangle, top. Letters represent the locations for which poststimulus time histograms are shown below and bar graphs quantify the firing rates at each of the 3 stimulus conditions; ii values are also depicted. For the location represented by A ii = 75.23% and is statistically significant (*P = 0.0001). For the location represented by B ii = 130.81% and is statistically significant (*P = 0.0001). For the location represented by C ii = 11.52% and is statistically nonsignificant. The same is true for the location represented by D, where ii = 6.4% and P = 0.67.

Fig. 3.

Multisensory neurons in the SC exhibit different response durations: short discharge durations and long discharge durations. Short discharge duration is associated with high integrative abilities (mean ii = 92.43%), while long discharge duration is associated with lower integrative abilities (mean ii = 34.35%, R = −0.19, P < 0.00001). Solid black line represents the trend of the data set (y = −0.0828x + 87.474).

Fig. 4.

Relationship between best unisensory and multisensory response durations. A: for response enhancements, multisensory response duration was significantly longer (mean = 225.08 ms) than the best unisensory condition (mean = 135.79 ms) as measured by the Wilcoxon signed-rank test (P < 0.00001). Solid black line represents the trend of the data set, while dashed black line represents the slope of 1 (y = x). B: for response depressions, the multisensory duration was significantly lower (mean = 82.55 ms) than the best unisensory duration (mean = 180.94 ms) (P < 0.00001). Solid black line represents the slope of the data, which is <1, while dashed line has a slope of 1 (y = x). C: for no interactions, the dashed line representing a slope of 1 and the trend of the data set represented by the solid black line overlap and the durations do not differ between the best unisensory (mean = 245.49 ms) and multisensory (mean = 251.22 ms) conditions (P = 0.06).

Fig. 5.

ii is plotted for locations with short discharge duration and locations with long discharge duration of a single neuron (coded by symbols) for a subset of 10 representative neurons. It can be seen from this graph that the same cell with short response duration exhibits higher integrative abilities than with long response duration when the integrative ability of the neuron is very low.

Fig. 6.

Mean statistical contrast (msc) as a function of multisensory duration. Locations with short response durations are mostly associated with statistically significant (P < 0.05 as tested by Wilcoxon rank test) superadditive and subadditive interactions (shown by black dots), while locations with long discharge durations are mostly associated with msc values that are statistically not significant (P > 0.05 as tested by Wilcoxon rank test) (shown by gray dots). Solid black line represents the mean msc value (1.34) for short discharge durations, while dashed line represents the mean msc value (0.17) for the longer response durations.

Fig. 7.

Relationship between multisensory firing rate and multisensory duration of response. Overall short discharge duration (filled circles) is accompanied by high firing rates, while long discharge durations (open circles) are accompanied by low firing rates (R = −0.39, P = 0.009). Horizontal solid line represents the mean firing rate for short discharge durations (41.5 spikes/s), which is significantly higher than the mean firing rate for long responses (horizontal dashed line, 27.5 spikes/s) (t-test, P = 0.0085).

Fig. 8.

Phases of integration: contrast measures for the early, middle, and late phases of integration for the long discharge duration of a subset of neurons. The early phase is characterized by superadditive interactions, while the middle and late phases are characterized by additive interactions. Black circles represent statistically significant msc values (P < 0.05), while gray circles represent nonsignificant values as measured by Wilcoxon rank test.