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M T Wallace

Publications and source records attributed to M T Wallace.

At least 19 recordsLinked to original sources

Unifying multisensory signals across time and space.

The brain integrates information from multiple sensory modalities and, through this process, generates a coherent and apparently seamless percept of the external world. Although multisensory integration typically binds information that is derived from the same event, when multisensory cues are somewhat discordant they can result in illusory percepts such as the "ventriloquism effect." These biases in stimulus localization are generally accompanied by the perceptual unification of the two stimuli. In the current study, we sought to further elucidate the relationship between localization biases, perceptual unification and measures of a participant's uncertainty in target localization (i.e., variability). Participants performed an auditory localization task in which they were also asked to report on whether they perceived the auditory and visual stimuli to be perceptually unified. The auditory and visual stimuli were delivered at a variety of spatial (0 degrees, 5 degrees, 10 degrees, 15 degrees ) and temporal (200, 500, 800 ms) disparities. Localization bias and reports of perceptual unity occurred even with substantial spatial (i.e., 15 degrees ) and temporal (i.e., 800 ms) disparities. Trial-by-trial comparison of these measures revealed a striking correlation: regardless of their disparity, whenever the auditory and visual stimuli were perceived as unified, they were localized at or very near the light. In contrast, when the stimuli were perceived as not unified, auditory localization was often biased away from the visual stimulus. Furthermore, localization variability was significantly less when the stimuli were perceived as unified. Intriguingly, on non-unity trials such variability increased with decreasing disparity. Together, these results suggest strong and potentially mechanistic links between the multiple facets of multisensory integration that contribute to our perceptual Gestalt.

Acoustic Stimulation↗

Superior colliculus lesions preferentially disrupt multisensory orientation.

The general involvement of the superior colliculus (SC) in orientation behavior and the striking parallels between the multisensory responses of SC neurons and overt orientation behaviors have led to assumptions that these neural and behavioral changes are directly linked. However, deactivation of two areas of cortex which also contain multisensory neurons, the anterior ectosylvian sulcus and rostral lateral suprasylvian sulcus have been shown to eliminate multisensory orientation behaviors, suggesting that this behavior may not involve the SC. To determine whether the SC contributes to this behavior, cats were tested in a multisensory (i.e. visual-auditory) orientation task before and after excitotoxic lesions of the SC. For unilateral SC lesions, modality-specific (i.e. visual or auditory) orientation behaviors had returned to pre-lesion levels after several weeks of recovery. In contrast, the enhancements and depressions in behavior normally seen with multisensory stimuli were severely compromised in the contralesional hemifield. No recovery of these behaviors was observed within the 6 month testing period. Immunohistochemical labeling of the SC revealed a preferential loss of parvalbumin-immunoreactive pyramidal neurons in the intermediate layers, a presumptive multisensory population that targets premotor areas of the brainstem and spinal cord. These results highlight the importance of the SC for multisensory behaviors, and suggest that the multisensory orientation deficits produced by cortical lesions are a result of the loss of cortical influences on multisensory SC neurons.

Animals↗

Visual localization ability influences cross-modal bias.

The ability of a visual signal to influence the localization of an auditory target (i.e., "cross-modal bias") was examined as a function of the spatial disparity between the two stimuli and their absolute locations in space. Three experimental issues were examined: (a) the effect of a spatially disparate visual stimulus on auditory localization judgments; (b) how the ability to localize visual, auditory, and spatially aligned multisensory (visual-auditory) targets is related to cross-modal bias, and (c) the relationship between the magnitude of cross-modal bias and the perception that the two stimuli are spatially "unified" (i.e., originate from the same location). Whereas variability in localization of auditory targets was large and fairly uniform for all tested locations, variability in localizing visual or spatially aligned multisensory targets was much smaller, and increased with increasing distance from the midline. This trend proved to be strongly correlated with biasing effectiveness, for although visual-auditory bias was unexpectedly large in all conditions tested, it decreased progressively (as localization variability increased) with increasing distance from the midline. Thus, central visual stimuli had a substantially greater biasing effect on auditory target localization than did more peripheral visual stimuli. It was also apparent that cross-modal bias decreased as the degree of visual-auditory disparity increased. Consequently, the greatest visual-auditory biases were obtained with small disparities at central locations. In all cases, the magnitude of these biases covaried with judgments of spatial unity. The results suggest that functional properties of the visual system play the predominant role in determining these visual-auditory interactions and that cross-modal biases can be substantially greater than previously noted.

Adult↗

Sensory and multisensory responses in the newborn monkey superior colliculus.

Superior colliculus (SC) neurons have the ability to synthesize information from different sensory modalities, resulting in enhancements (or depressions) of their activity. This physiological capacity is, in turn, closely tied to changes in overt attentive and orientation responses. The present study shows that, in contrast to more altricial species, many deep layer SC neurons in the rhesus monkey are multisensory at birth. Such neurons can respond to stimuli from different sensory modalities, and all convergence patterns seen in the adult are represented. Nevertheless, these neurons cannot yet synthesize their multisensory inputs. Rather, they respond to combinations of cross-modal stimuli much like they respond to their individual modality-specific components. This immature property of multisensory neurons is in contrast to many of the surprisingly sophisticated modality-specific response properties of these neurons and of their modality-specific neighbors. Thus, although deep SC neurons in the newborn have longer latencies and larger receptive fields than their adult counterparts, they are already highly active and are distributed in the typical adult admixture of visual, auditory, somatosensory, and multisensory neurons. Furthermore, the receptive fields of these neurons are already ordered into well organized topographic maps, and the different receptive fields of the same multisensory neurons show a good degree of cross-modal spatial register. These data, coupled with those from cat, suggest that the capacity to synthesize multisensory information does not simply appear in SC neurons at a prescribed maturational stage but rather develops only after substantial experience with cross-modal cues.

Acoustic Stimulation↗

The influence of visual and auditory receptive field organization on multisensory integration in the superior colliculus.

The spatial register of the different receptive fields of multisensory neurons in the superior colliculus (SC) plays a significant role in determining the responses of these neurons to cross-modal stimulus combinations. Spatially coincident visual-auditory stimuli fall within these overlapping receptive fields and generally produce response enhancements that exceed the individual modality-specific responses and can exceed their sum. Yet, in this context, it has not been clear how "spatial coincidence" is operationally defined. Given the large size of SC receptive fields, visual and auditory stimuli could be within their respective receptive fields even when there are substantial spatial disparities between them. Indeed, previous observations have raised the possibility that there may be a second level of determinism in how SC neurons deal with the relative spatial locations of within-field cross-modal stimuli; specifically, that multisensory response enhancements become progressively weaker as the within-field visual and auditory stimuli become increasingly disparate. While the present experiments demonstrated that SC multisensory neurons have heterogeneous receptive fields, and that the greatest number of impulses evoked were by stimuli that fell within the area of cross-modal receptive field overlap, they also indicate that there is no systematic relationship between cross-modal stimulus disparity and the magnitude of multisensory response enhancement. Thus, two within-field cross-modal stimuli produced the same proportionate change (i.e., multisensory response enhancement) when they were widely disparate as they did when they overlapped one another in space. These observations indicate that cross-modal spatial coincidence can be defined operationally by the borders of an SC neuron's receptive fields regardless of the size of those receptive fields and/or the absolute spatial disparity between within-field cross-modal stimuli.

Acoustic Stimulation↗

Nonvisual influences on visual-information processing in the superior colliculus.

Although visually responsive neurons predominate in the deep layers of the superior colliculus (SC), the majority of them also receive sensory inputs from nonvisual sources (i.e. auditory and/or somatosensory). Most of these 'multisensory' neurons are able to synthesize their cross-modal inputs and, as a consequence, their responses to visual stimuli can be profoundly enhanced or depressed in the presence of a nonvisual cue. Whether response enhancement or response depression is produced by this multisensory interaction is predictable based on several factors. These include: the organization of a neuron's visual and nonvisual receptive fields; the relative spatial relationships of the different stimuli (to their respective receptive fields and to one another); and whether or not the neuron is innervated by a select population of cortical neurons. The response enhancement or depression of SC neurons via multisensory integration has significant survival value via its profound impact on overt attentive/orientation behaviors. Nevertheless, these multisensory processes are not present at birth, and require an extensive period of postnatal maturation. It seems likely that the sensory experiences obtained during this period play an important role in crafting the processes underlying these multisensory interactions.

Acoustic Stimulation↗

Two cortical areas mediate multisensory integration in superior colliculus neurons.

The majority of multisensory neurons in the cat superior colliculus (SC) are able to synthesize cross-modal cues (e.g., visual and auditory) and thereby produce responses greater than those elicited by the most effective single modality stimulus and, sometimes, greater than those predicted by the arithmetic sum of their modality-specific responses. The present study examined the role of corticotectal inputs from two cortical areas, the anterior ectosylvian sulcus (AES) and the rostral aspect of the lateral suprasylvian sulcus (rLS), in producing these response enhancements. This was accomplished by evaluating the multisensory properties of individual SC neurons during reversible deactivation of these cortices individually and in combination using cryogenic deactivation techniques. Cortical deactivation eliminated the characteristic multisensory response enhancement of nearly all SC neurons but generally had little or no effect on a neuron's modality-specific responses. Thus, the responses of SC neurons to combinations of cross-modal stimuli were now no different from those evoked by one or the other of these stimuli individually. Of the two cortical areas, AES had a much greater impact on SC multisensory integrative processes, with nearly half the SC neurons sampled dependent on it alone. In contrast, only a small number of SC neurons depended solely on rLS. However, most SC neurons exhibited dual dependencies, and their multisensory enhancement was mediated by either synergistic or redundant influences from AES and rLS. Corticotectal synergy was evident when deactivating either cortical area compromised the multisensory enhancement of an SC neuron, whereas corticotectal redundancy was evident when deactivation of both cortical areas was required to produce this effect. The results suggest that, although multisensory SC neurons can be created as a consequence of a variety of converging tectopetal afferents that are derived from a host of subcortical and cortical structures, the ability to synthesize cross-modal inputs, and thereby produce an enhanced multisensory response, requires functional inputs from the AES, the rLS, or both.

Acoustic Stimulation↗

Onset of cross-modal synthesis in the neonatal superior colliculus is gated by the development of cortical influences.

Many neurons in the superior colliculus (SC) are able to integrate combinations of visual, auditory, and somatosensory stimuli, thereby markedly affecting the vigor of their responses to external stimuli. However, this capacity for multisensory integration is not inborn. Rather, it appears comparatively late in postnatal development and is not expressed until the SC passes through several distinct developmental stages. As shown here, the final stage in this sequence is one in which a region of association cortex establishes functional control over the SC, thus enabling the multisensory integrative capabilities of its target SC neurons. The first example of this corticotectal input was seen at postnatal day 28. For any individual SC neuron, the onset of corticotectal influences appeared to be abrupt. Because this event occurred at very different times for different SC neurons, a period of 3-4 postnatal months was required before the adult-like condition was achieved. The protracted postnatal period required for the maturation of these corticotectal influences corresponded closely with estimates of the peak period of cortical plasticity, raising the possibility that the genesis of these corticotectal influences, and hence the onset of SC multisensory integration, occurs only after the cortex is capable of exerting experience-dependent control over SC neurons.

Algorithms↗

Multisensory integration in the superior colliculus of the alert cat.

The modality convergence patterns, sensory response properties, and principles governing multisensory integration in the superior colliculus (SC) of the alert cat were found to have fundamental similarities to those in anesthetized animals. Of particular interest was the observation that, in a manner indistinguishable from the anesthetized animal, combinations of two different sensory stimuli significantly enhanced the responses of SC neurons above those evoked by either unimodal stimulus. These observations are consistent with the speculation that there is a functional link among multisensory integration in individual SC neurons and cross-modality attentive and orientation behaviors.

Acoustic Stimulation↗

Development of multisensory neurons and multisensory integration in cat superior colliculus.

The development of multisensory neurons and multisensory integration was examined in the deep layers of the superior colliculus of kittens ranging in age from 3 to 135 d postnatal (dpn). Despite the high proportion of multisensory neurons in adult animals, no such neurons were found during the first 10 d of postnatal life. Rather, all sensory-responsive neurons were unimodal. The first multisensory neurons (somatosensory-auditory) were found at 12 dpn, and visually responsive multisensory neurons were not found until 20 dpn. Early multisensory neurons responded weakly to sensory stimuli, had long latencies, large receptive fields, and poorly developed response selectivities. Most surprising, however, was their inability to integrate combinations of sensory cues to produce significant response enhancement (or depression), a characteristic feature of the adult. Responses to combinations of sensory cues differed little from responses to their modality-specific components. At 28 dpn an abrupt physiological change was noted. Some multisensory neurons now integrated combinations of cross-modality cues and exhibited significant response enhancements when these cues were spatially coincident and response depressions when the cues were spatially disparate. During the next 2 months the incidence of multisensory neurons, and the proportion of these neurons capable of adult-like multisensory integration, gradually increased. Once multisensory integration appeared in a given neuron, its properties changed little with development. Even the youngest integrating neurons showed superadditive enhancements and spatial characteristics of multisensory integration that were indistinguishable from the adult. Nevertheless, neonatal and adult multisensory neurons differed in the manner in which they integrated temporally asynchronous stimuli, a distribution that may reflect the very different behavioral requirements at different ages. The possible maturational role of corticotectal projections in the abrupt gating of multisensory integration is discussed.

Acoustic Stimulation↗

Visual response properties and visuotopic representation in the newborn monkey superior colliculus.

Visual response properties and visuotopic representation in the newborn monkey superior colliculus. J. Neurophysiol. 78: 2732-2741, 1997. Visually responsive neurons were recorded in the superior colliculus (SC) of the newborn rhesus monkey. The receptive fields of these neurons were larger than those in the adult, but already were organized into a well-ordered map of visual space that was very much like that seen in mature animals. This included a marked expansion of the representation of the central 10 degrees of the visual field and a systematic foveal to peripheral increase in receptive field size. Although newborn SC neurons had longer response latencies than did their adult counterparts, they responded vigorously to visual stimuli and exhibited many visual response properties that are characteristic of the adult. These included surround inhibition, within-field spatial summation, within-field spatial inhibition, binocularity, and an adult-like ocular dominance distribution. As in the adult, SC neurons in the newborn preferred a moving visual stimulus and had adult-like selectivities for stimulus speed. The developmentally advanced state of the functional circuitry of the newborn monkey SC contrasts with the comparative immaturity of neurons in its visual cortex. It also contrasts with observations on the state of maturation of the newborn SC in other developmental models (e.g., cat). The observation that extensive visual experience is not necessary for the development of many adult-like SC response properties in the monkey SC may help explain the substantial visual capabilities shown by primates soon after birth.

Aging↗

Mechanisms of within- and cross-modality suppression in the superior colliculus.

The present studies were initiated to explore the basis for the response suppression that occurs in cat superior colliculus (SC) neurons when two spatially disparate stimuli are presented simultaneously or in close temporal proximity to one another. Of specific interest was examining the possibility that suppressive regions border the receptive fields (RFs) of unimodal and multisensory SC neurons and, when activated, degrade the neuron's responses to excitatory stimuli. Both within- and cross-modality effects were examined. An example of the former is when a response to a visual stimulus within its RF is suppressed by a second visual stimulus outside the RF. An example of the latter is when the response to a visual stimulus within the visual RF is suppressed when a stimulus from a different modality (e. g., auditory) is presented outside its (i.e., auditory) RF. Suppressive regions were found bordering visual, auditory, and somatosensory RFs. Despite significant modality-specific differences in the incidence and effectiveness of these regions, they were generally quite potent regardless of the modality. In the vast majority (85%) of cases, responses to the excitatory stimulus were degraded by >/=50% by simultaneously stimulating the suppressive region. Contrary to expectations and previous speculations, the effects of activating these suppressive regions often were quite specific. Thus powerful within-modality suppression could be demonstrated in many multisensory neurons in which cross-modality suppression could not be generated. However, the converse was not true. If an extra-RF stimulus inhibited center responses to stimuli of a different modality, it also would suppress center responses to stimuli of its own modality. Thus when cross-modality suppression was demonstrated, it was always accompanied by within-modality suppression. These observations suggest that separate mechanisms underlie within- and cross-modality suppression in the SC. Because some modality-specific tectopetal structures contain neurons with suppressive regions bordering their RFs, the within-modality suppression observed in the SC simply may reflect interactions taking place at the level of one input channel. However, the presence of modality-specific suppression at the level of one input channel would have no effect on the excitation initiated via another input channel. Given the modality-specificity of tectopetal inputs, it appears that cross-modality interactions require the convergence of two or more modality-specific inputs onto the same SC neuron and that the expression of these interactions depends on the internal circuitry of the SC. This allows a cross-modality suppressive signal to be nonspecific and to degrade any and all of the neuron's excitatory inputs.

Acoustic Stimulation↗

Comparisons of cross-modality integration in midbrain and cortex.

Multisensory neurons are abundant in the superior colliculus and anterior ectosylvian cortex of the cat. Despite the fact that these areas receive inputs from different regions, and are likely to be involved in different functional roles, there multisensory neurons have many fundamental similarities. They all have multiple receptive fields, one for each sensory input, and these receptive fields overlap one another. It is this spatial correspondence among receptive fields that determines the manner in which both populations of neurons integrate the inputs they receive from different sensory channels. Several principles of integration characterize both cortical and midbrain multisensory neurons, and these constancies in the fundamentals of cross-modality integration are likely to provide a basis for coherence at different levels of the neuraxis. Yet there are also obvious differences in these populations of multisensory neurons. Cortical receptive fields are significantly larger than those in the midbrain, have a lower incidence of suppressive surrounds, and exhibit less cross-modality inhibitory interactions than in the midbrain. Presumably, these differences reflect a greater emphasis on non-spatial aspects of cross-modality integration in cortex than is required by the orientation and localization functions mediated by the superior colliculus.

Animals↗

Sensory organization of the superior colliculus in cat and monkey.

The sensory representations and response properties of neurons in the multisensory layers of the superior colliculus (SC) of the cat and monkey are strikingly similar. In both species, significant numbers of unimodal visual, auditory, and somatosensory neurons are intermixed, and share modality-specific stimulus selectivities. In addition, these neurons have receptive fields that are organized in similar map-like representations, with the different maps sharing the same axes and, thus, exhibiting a characteristic cross-modality correspondence. Both species also have a large contingent of multisensory neurons that synthesize information from different sensory modalities using a common set of spatial, temporal, and physical principles. These findings suggest that, despite differences in the ontogeny and behavioral repertoires of cat and monkey, there is a substantial conservation in the organization and functional properties of SC neurons. Apparently, these functional features of the SC are adaptive in a wide variety of ecological situations.

Animals↗

Representation and integration of multiple sensory inputs in primate superior colliculus.

1. The properties of visual-, auditory-, and somatosensory-responsive neurons, as well as of neurons responsive to multiple sensory cues (i.e., multisensory), were examined in the superior colliculus of the rhesus monkey. Although superficial layer neurons responded exclusively to visual stimuli and visual inputs predominated in deeper layers, there was also a rich nonvisual and multisensory representation in the superior colliculus. More than a quarter (27.8%) of the deep layer population responded to stimuli from more than a single sensory modality. In contrast, 37% responded only to visual cues, 17.6% to auditory cues, and 17.6% to somatosensory cues. Unimodal- and multisensory-responsive neurons were clustered by modality. Each of these modalities was represented in map-like fashion, and the different representations were in alignment with one another. 2. Most deep layer visually responsive neurons were binocular and exhibited poor selectivity for such stimulus characteristics as orientation, velocity, and direction of movement. Similarly, most auditory-responsive neurons had contralateral receptive fields and were binaural, but had little frequency selectivity and preferred complex, broad-band sounds. Somatosensory-responsive neurons were overwhelmingly contralateral, high velocity, and rapidly adapting. Only rarely did somatosensory-responsive neurons require distortion of subcutaneous tissue for activation. 3. The spatial congruence among the different receptive fields of multisensory neurons was a critical feature underlying their ability to synthesize cross-modal information. 4. Combinations of stimuli could have very different consequences in the same neuron, depending on their temporal and spatial relationships. Generally, multisensory interactions were evident when pairs of stimuli were separated from one another by < 500 ms, and the products of these interactions far exceeded the sum of their unimodal components. Whether the combination of stimuli produced response enhancement, response depression, or no interaction depended on the location of the stimuli relative to one another and to their respective receptive fields. Maximal response enhancements were observed when stimuli originated from similar locations in space (as when derived from the same event) because they fell within the excitatory receptive fields of the same multisensory neurons. If, however, the stimuli were spatially disparate such that one fell beyond the excitatory borders of its receptive field, either no interaction was produced or this stimulus depressed the effectiveness of the other. Furthermore, maximal response interactions were seen with the pairing of weakly effective unimodal stimuli. As the individual unimodal stimuli became increasingly effective, the levels of response enhancement to stimulus combinations declined, a principle referred to as inverse effectiveness. Many of the integrative principles seen here in the primate superior colliculus are strikingly similar to those observed in the cat. These observations indicate that a set of common principles of multisensory integration is adaptable in widely divergent species living in very different ecological situations. 5. Surprisingly, a few multisensory neurons had individual receptive fields that were not in register with one another. This has not been noted in multisensory neurons of other species, and these "anomalous" receptive fields could present a daunting problem: stimuli originating from the same general location in space cannot simultaneously fall within their respective receptive fields, a stimulus pairing that may result in response depression. Conversely, stimuli that originate from separate events and disparate locations (and fall within their receptive fields) may result in response enhancement. However, the spatial principle of multisensory integration did not apply in these cases. (ABSTRACT TRUNCATED)

Animals↗

Cross-modal synthesis in the midbrain depends on input from cortex.

1. The synthesis of information from different sensory modalities in the superior colliculus is an important precursor of attentive and orientation behavior. 2. This integration of multisensory information is critically dependent on inputs from a small area of association cortex, the anterior ectosylvian sulcus. Removal of these corticotectal influences can have a remarkably specific effect: it can eliminate multisensory integration in superior colliculus neurons while leaving their responses to unimodal cues intact. 3. Apparently, some of the associative functions of cortex are accomplished via its target neurons in the midbrain.

Animals↗