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NEUROREPORT STANFORD AND STEIN so superadditivi ty might not be a stable feature of a neuron, but dependent of the properties of the stimuli. enhancements. Doing so has been particularly valuable, if not essential, for assessing how normal development [18,19], altered sensory experience [20], or acute perturbations of input (e.g. cortical inactivation) [21] affect the incidence of multisensory integration within the superior colliculus, but with the untoward effect of creating a biased representation of superior colliculus multisensory interactions within the literature. In an effort to more fully characterize the nature of multisensory integration for single neurons and populations of neurons within the cat superior colliculus, recent studies have eschewed the near-exclusive use of minimally effective stimuli in favor of parametric manipulations of stimulus intensity to modulate effectiveness over a broad range. In one such study, Stanford et al. [22] quantitatively evaluated the operation performed by superior colliculus multisensory neurons for combinations of modality-specific stimuli covering a wide range of efficacies. Consistent with the many individual examples in the literature (e.g. see Figs 1 and 2c) this study verified that superadditivity is in fact commonly observed when very ineffective modality-specific stimuli are combined. They also, however, found that the incidence of superadditive interactions fell precipitously with increasing efficacy of the individual modality-specific stimulus components. Indeed, across the broader range of efficacies, the majority of the interactions in their sample approximated linear summation of the modality-specific inputs, with superadditive and subadditive interactions defining the tails of a normal distribution (Fig. 3). Analogous results were described by Perrault et al. [23], who also evaluated multisensory interactions against a benchmark of additivity with emphasis on relationships between the multisensory operation and the dynamic ranges of individual superior colliculus neurons. The results were once again consistent with extant examples in the literature, but also established the context in which such previous examples should be considered. Perrault et al. [23] demonstrated that weakly responsive neurons with very compressed dynamic ranges (i.e. weakly responsive over a broad range of stimulus intensities) were those most likely to demonstrate superadditivity exclusively, whereas those with more expansive and more linear dynamic ranges tended to transition from superadditivity to additivity or from additivity to subadditivity as stimulus intensity (and efficacy) increased. These recent studies demonstrated that, in the superior colliculus at least, superadditivity is but one facet of multisensory integration, and one that is produced under a very circumscribed range of circumstances, specifically when the unisensory stimuli to be combined are weakly effective. As one might have expected, the results of these studies illustrate that the principle of ‘inverse effectiveness’ can be extended beyond multisensory enhancement to include the form of the multisensory computation. These larger surveys of superior colliculus integration are particularly germane to consideration of an earlier study by Populin and Yin [24], which stands out as the only proponent of a contrarian and rather provocative conjecture that superadditivity is an artifact of the anesthetic agent used in most previous studies. This conclusion was based on the fact that in their study of multisensory integration in the superior colliculus of alert cats, Populin and Yin found little evidence of superadditivity, instead reporting that most multisensory interactions were either additive (linear) Response mode proportion 100 80 60 40 20 0 0−2 2−4 4−6 6−8 Superadditive Additive Subadditive 8−10 10−12 12−14 Unisensory response sum (impulses/trial) Fig. 3 The incidence of superadditivity declines rapidly with increasing stimulus strength. Shown here, in a ¢gure adapted from Figure 6a of Stanford et al. [22], is an illustration of how the neural integration of crossmodal stimulus pairs depends on the strength of the modality-speci¢c component stimuli. In this experiment, single neuron activity from the cat superior colliculus was recorded in response to visual, auditory, and visual-auditory stimuli across a wide range of stimulus intensities. In each case, the magnitude of the response to the cross-modal stimulus was evaluated with respect to a benchmark of simple summation of the responses to the modality-speci¢c component stimuli (see Stanford et al. [22] for details).The plot illustrates the relative likelihood of multisensory responses that exceeded summation (superadditive¼¢lled circles), failed to achieve summation (subadditive¼open squares), or were consistent with summation (additive¼open circles). Note that the likelihood of observing superadditivity fell dramatically as the e⁄cacy of the component stimuli increased. Thus, superadditivity predominated only for very weakly e¡ective auditory and visual stimulus components, stimuli for which the predicted sum of the modality-speci¢c responses failed to exceed 2^ 4 impulses/trial. or subadditive (sublinear). Although the Populin and Yin findings appeared to be an extreme departure from earlier literature, including those from other studies in awake animals (e.g. see Ref. [25]), their data overlap greatly with the more recent studies showing that, in anesthetized cats, additivity predominates for combinations of all but the weakest modality-specific stimuli [22,23]. Populin and Yin do not relate integration mode to stimulus efficacy for their sample; however, the specific examples provided suggest moderate efficacy and, at first glance, seem in line with the most recent results from anesthetized cats. This, along with both earlier [25] and more recent reports of superadditive multisensory interactions in single neurons in a variety of structures in awake, behaving animals (monkey cortex: [26]; rat thalamus: [27]), coupled with the data from fMRI and ERP studies (see above) strongly suggest that a difference in sampling and/or stimulus efficacy is the more parsimonious explanation of the extreme paucity of superadditive cases in their sample. Implications for behavior From a functional perspective, the issue of integrative mechanism (i.e. linear or nonlinear) is relevant only to the extent that it dictates the magnitude (and/or timing) of the postsynaptic response. Neurons in the superior colliculus represent salient visual, auditory, and tactile stimuli and contribute to the formation of motor commands to orient even if a certain % of trials with superadd, that would manifest as increased activity in study.. 79 0 Vol 18 No 8 28 May 2007 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
SUPERADDITIVITY IN MULTISENSORY INTEGRATION NEUROREPORT 1.0 Saccadic RT and inverse effectiveness 12.0 Manual RT and inverse effectiveness Normalized (re: visual) RT 0.8 0.6 0.4 0.2 Vis Aud V + A Percentage of reduction in RT 10.0 8.0 6.0 4.0 2.0 VA low T low A low VA high VT low T high A high VT high 0.0 −21 dB −18 dB −12 dB −6 dB Auditory signal to noise ratio Fig. 4 Saccadic reaction time and inverse e¡ectiveness. This ¢gure, which was adapted from Figure 10 of Corneil et al. [7], illustrates the relationship between stimulus strength and the decrements in saccadic reaction time (RT) resulting from combining visual and auditory stimuli. Human individuals were instructed to make saccades as quickly as possible to a visual stimulus, an auditory stimulus, or a spatially congruent visual^auditory stimulus. Auditory stimuli were presented at di¡erent signal strengths ( 21, 18, 12, and 6 dB) with respect to background noise. Plotted are mean RTs for saccades to the auditory stimulus alone (white bars) and the auditory^visual stimulus pair (gray bars) as a function of increasing auditory signal strength. All mean RTs are normalized relative to that for saccades to the visual stimulus alone (black bars ^ value of 1.0). As expected, mean RT for the auditory stimulus (white bars) declines monotonically as a function of increasing auditory stimulus strength (increasing S/N ratio from left to right). Note, however, that S/N noise ratio also modulates the in£uence of multisensory integration such that mean RT for the cross-modal pair (gray bars) is shorter than that for the auditory stimulus alone (white bars) for the weakest auditory stimulus ( 21dB), but not for the most intense auditory stimulus ( 6 dB), a ¢nding consistent with inverse e¡ectiveness. It is also important to note that the apparent RT bene¢ts associated with cross-modal stimuli were not exclusive to the lowest S/N ratio, but appear to be present and of intermediate magnitude for the intermediate S/N ratios ( 12 and 18 dB). (eyes, head, ears, body) to these stimuli (see [28,29] for reviews). It is reasonable to presume that any stimulusrelated factor that leads to an augmented neural response in the superior colliculus also increases the salience of that stimulus, and with it the probability that it will elicit an orienting response. It is well established that highly salient stimuli (e.g. bright, loud) provoke behavioral responses more reliably and more rapidly. Furthermore, these same stimuli evoke neural responses that are of shorter latency, more vigorous, and less variable whether considered from the perspective of a single neuron or populations of neurons. In many instances, it seems justified to infer a causal relationship from such behavior/neural correlates (e.g. greater activity level, shorter reaction time). Considering superadditivity as a context-limited phenomenon within the broader spectrum of multisensory interactions, it seems self-evident that multisensory behavioral phenomena, at least those mediated by the superior colliculus, are not wholly dependent on supralinear interactions between the senses. Whereas one might reasonably expect that such interactions contribute to the most potent behavioral effects observed when very weak unisensory stimuli are combined, it should be recognized that simple 0.0 V+A V+T T+A Fig. 5 Manual reaction times and inverse e¡ectiveness. Shown here are the decrements in manual reaction time (RT) resulting from the addition of a stimulus from a second modality (i.e. cross-modal versus modalityspeci¢c). They are inversely related to stimulus intensity. The data are taken fromTable 4 of Diederich and Colonius [6]. In their experiment, human individuals were instructed to depress a response button with each hand upon detecting any stimulus, and manual reaction times were measured. Stimuli consisted of a visual £ash, auditory pure tone, vibratory tactile stimulus, or some combination of these three stimuli. Plotted are the % reductions in RT for the visual^auditory, tactile^visual, and tactile^ auditory stimulus combinations. For each pairing, the percent reduction in mean RT is plotted with reference to that for the modality-speci¢c component stimulus that yielded the shortest mean RTaccording to the general formula: % reduction in RT¼min(RT 1 , RT 2 ) (RT 1 + 2 )/min(RT 1 , RT 2 ) 100, where RT 1 and RT 2 are mean RTs for responses to each of the stimulus components and RT 1 + 2 is the mean RT for responses to the stimulus combination. Note that for each cross-modal stimulus, the higher intensity combination (gray bars) yielded a proportionally lower reduction in RT than did the lower intensity combination (black bars), thus illustrating that the concept of inverse e¡ectiveness applies to manual RT. Note also that all stimuli were suprathreshold, illustrating that the behavioral bene¢ts for multisensory integration are not exclusive to near threshold stimulation and that behavioral bene¢ts, albeit attenuated, are also observed for higher intensity combinations. Stimulus pairings VA low , VA high , VT low , VT high , T low A low , T high A high correspond to VA 70 , VA 90 , T 1 V, T 3 V,T 1 A 70 ,T 3 A 90 , respectively. summation, and even sublinear combinations, of independent inputs would be expected to have behavioral manifestations by virtue of yielding substantial increases in superior colliculus activity. The predicted inverse trend has been demonstrated empirically for behavior; the influence of combining stimuli on behavioral measures such as localization or reaction time does, in fact, decrease with increasing salience of the unisensory components, and this principle seems to apply equally well to orientation of gaze (e.g. [7]; see Fig. 4) or limb movement (e.g. [6]; see Fig. 5). Note, however, that the examples depicted in these illustrations suggest that the behavioral effects of multisensory integration, whereas certainly greatest for the weakest stimuli, are not exclusive to such combinations. The concept of inverse effectiveness as it applies to behavior is intuitive and, as discussed above, an analog (and perhaps its neural correlate) is evident in the responses of superior colliculus multisensory neurons: combinations of very weakly effective modality-specific stimuli result in proportionately larger enhancements than do combinations of highly effective stimuli (see Figs 1–3). Given that multisensory phenomena arise via convergence (and, in Vol 18 No 8 28 May 2007 791 Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
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