Evaluating the operations underlying multisensory integration in the cat superior colliculus

Abstract

It is well established that superior colliculus (SC) multisensory neurons integrate cues from different senses; however, the mechanisms responsible for producing multisensory responses are poorly understood. Previous studies have shown that spatially congruent cues from different modalities (e.g., auditory and visual) yield enhanced responses and that the greatest relative enhancements occur for combinations of the least effective modality-specific stimuli. Although these phenomena are well documented, little is known about the mechanisms that underlie them, because no study has systematically examined the operation that multisensory neurons perform on their modality-specific inputs. The goal of this study was to evaluate the computations that multisensory neurons perform in combining the influences of stimuli from two modalities. The extracellular activities of single neurons in the SC of the cat were recorded in response to visual, auditory, and bimodal visual-auditory stimulation. Each neuron was tested across a range of stimulus intensities and multisensory responses evaluated against the null hypothesis of simple summation of unisensory influences. We found that the multisensory response could be superadditive, additive, or subadditive but that the computation was strongly dictated by the efficacies of the modality-specific stimulus components. Superadditivity was most common within a restricted range of near-threshold stimulus efficacies, whereas for the majority of stimuli, response magnitudes were consistent with the linear summation of modality-specific influences. In addition to providing a constraint for developing models of multisensory integration, the relationship between response mode and stimulus efficacy emphasizes the importance of considering stimulus parameters when inducing or interpreting multisensory phenomena.

Figure 1.

The responses of a single SC neuron to visual, auditory, and multisensory stimuli. Rasters and PSTHs compose a matrix with responses to three intensities (low, medium, high) of modality-specific visual (left column) and modality-specific auditory (top row) stimuli (open histograms). Responses to the nine possible multisensory combinations of these modality-specific stimuli fill in the cells of the matrix (filled histograms within box outline) according to the usual convention (e.g., histogram LL depicts the response to combination of the low-intensity visual and low-intensity auditory stimulus). All PSTHs are binned at a resolution of 10 ms and plotted on the same scales. Stimulus onset is at t = 0. Values corresponding to the mean number of impulses per trial and the SDs are given for selected histograms (see text for details). Impulse rates (y-axis) are computed as number impulses per bin width (10 ms) × 100. Med, Medium.

Figure 2.

Generating the predicted multisensory sum. Visual, auditory, and multisensory responses and the distributions of predicted sums are shown for three different SC neurons (A-C). Left column, Rasters of impulses are shown for each trial of visual (left), auditory (middle), and visual-auditory multisensory (right) stimulation. In all cases, stimulus onset occurs at t = 0.5 s (first vertical gray line). Impulse counts were based on the 500 ms period from stimulus on set to t = 1 s (second vertical gray line). Right column, Probability density functions (pdf) of the predicted mean multisensory responses (mean number of impulses per trial) based on summing the modality-specific visual and auditory responses (see text for details). Gray arrow, Mean of the predicted distribution; black arrow, Mean of the actual multisensory response shown in the left column. The predicted mean, actual mean observed, and their difference expressed in SDs (z score) are shown for each example neuron. A, Subadditive interaction. B, Additive interaction. C, Superadditive interaction. Pred., Predicted mean; Obs., actual mean observed.

Figure 3.

The majority of multisensory interactions are additive. A, Frequency distributions of z scores, including all stimulus combinations (n = 1482), are shown for all neurons (n = 41). Open bars plotz scores relating the actual multisensory responses to predicted sums that did not incorporate a corrective subtraction of spontaneous activity. Filled bars show the z scores relating the same multisensory responses to predicted sums that are corrected for spontaneous activity. B, Cumulative density functions of the same data shown in A illustrate the relative frequency of subadditivity, additivity, and superadditivity with (filled squares) and without (open circles) the correction for spontaneous activity. Vertical dotted lines at z score values of -1.96 and 1.96 indicate the points of transition from subadditivity to additivity (-1.96) and from additivity to superadditivity (1.96). For each neuron, a single estimate of mean spontaneous rate was obtained from the prestimulus epochs of all unisensory and multisensory trials. The rate was then converted to an impulse count by multiplying by the time interval over which impulses were counted (e.g., 500 ms) (see Fig. 2). The duplicated spontaneous term (see Results for details) was then eliminated by subtracting one-half of the number of spontaneous impulses from the visual and auditory responses before creating the distribution of all possible sums (see Fig. 2). Uncorrected for spontaneous activity, the relative percentages of subadditivity, additivity, and superadditivity were 24.6, 56.4, and 19%, respectively. Corrected for spontaneous activity, the relative percentages of subadditivity, additivity, and superadditivity were 6.8, 69.4, and 24.8%, respectively.

Figure 4.

Imposing criteria for efficacy yields populations enriched for superadditive interactions. Shown are frequency distributions of z scores including only conditions that met either of two criteria for the efficacy of the modality-specific channels (valid cases; see Results for details). Filled bars are cases in which multisensory enhancement was observed (i.e., the multisensory response was greater than the greatest unisensory response). Unfilled bars are cases in which statistically significant activity was observed in response to each of the unisensory stimuli presented alone, but enhancement was not observed when they were presented in combination. Vertical dotted lines at z score values of -1.96 and 1.96 indicate the points of transition from subadditivity to additivity (-1.96) and from additivity to superadditivity (1.96). super, Superadditivity; add, additivity; sub, subadditivity.

Figure 5.

The observed versus the predicted multisensory response. A scatter plot relates the observed multisensory responses (mean number of impulses per trial) to the predicted sums (mean number of impulses per trial) for all cases in which multisensory enhancement was observed. Black circles and gray squares indicate statistically significant superadditivity (SUPER; z > 1.96) and subadditivity (SUB; z < -1.96), respectively. The open circles indicate cases of additivity (ADD). The solid diagonal line represents equality. Inset, A cumulative function of the same data illustrates that 90% of all observations correspond to a predicted sum of 14 impulses (imp.) per trial (dotted vertical lines on main panel and inset) or less.

Figure 6.

The mode of multisensory integration varies as an inverse function of stimulus efficacy. A, The plot shows the relative probability of observing subadditivity (SUB), additivity (ADD), and superadditivity (SUPER) as a function of the predicted sum magnitude (mean number of impulses per trial). The larger symbols connected by solid lines correspond to cases in which multisensory enhancement was observed (n = 547). The smaller symbols connected by dotted lines correspond to all valid cases (for details, see text and Fig. 4 legend). B, A plot of z score versus predicted sum (mean number of impulses per trial) for the same data shown in A. The horizontal dotted line at z = 1.96 marks the transition from additivity to superadditivity, and the solid line marks z = 0.SDs are shown as bars (enhancement) and open rectangles (valid cases).

Figure 7.

A response matrix illustrating the predominantly superadditive interactions for a weakly responsive SC neuron. All conventions are the same as for Figure 1.