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.     

Multisensory processing in "unimodal" neurons: cross-modal subthreshold auditory effects in cat extrastriate visual cortex

Historically, the study of multisensory processing has examined the function of the definitive neuron type, the bimodal neuron. These neurons are excited by inputs from more than one sensory modality, and when multisensory stimuli are present, they can integrate their responses in a predictable manner. However, recent studies have revealed that multisensory processing in the cortex is not restricted to bimodal neurons. The present investigation sought to examine the potential for multisensory processing in nonbimodal (unimodal) neurons in the retinotopically organized posterolateral lateral suprasylvian (PLLS) area of the cat. Standard extracellular recordings were used to measure responses of all neurons encountered to both separate- and combined-modality stimulation. Whereas bimodal neurons behaved as predicted, the surprising result was that 16% of unimodal visual neurons encountered were significantly facilitated by auditory stimuli. Because these unimodal visual neurons did not respond to an auditory stimulus presented alone but had their visual responses modulated by concurrent auditory stimulation, they represent a new form of multisensory neuron: the subthreshold multisensory neuron. These data also demonstrate that bimodal neurons can no longer be regarded as the exclusive basis for multisensory processing.     

Cortical control of sound localization in the cat: unilateral cooling deactivation of 19 cerebral areas

We examined the ability of mature cats to accurately orient to, and approach, an acoustic stimulus during unilateral reversible cooling deactivation of primary auditory cortex (AI) or 1 of 18 other cerebral loci. After attending to a central visual stimulus, the cats learned to orient to a 100-ms broad-band, white-noise stimulus emitted from a central speaker or 1 of 12 peripheral sites (at 15 degrees intervals) positioned along the horizontal plane. Twenty-eight cats had two to six cryoloops implanted over multiple cerebral loci. Within auditory cortex, unilateral deactivation of AI, the posterior auditory field (PAF) or the anterior ectosylvian sulcus (AES) resulted in orienting deficits throughout the contralateral field. However, unilateral deactivation of the anterior auditory field, the second auditory cortex, or the ventroposterior auditory field resulted in no deficits on the orienting task. In multisensory cortex, unilateral deactivation of neither ventral or dorsal posterior ectosylvian cortices nor anterior or posterior area 7 resulted in any deficits. No deficits were identified during unilateral cooling of the five visual regions flanking auditory or multisensory cortices: posterior or anterior ii suprasylvian sulcus, posterior suprasylvian sulcus or dorsal or ventral posterior suprasylvian gyrus. In motor cortex, we identified contralateral orienting deficits during unilateral cooling of lateral area 5 (5L) or medial area 6 (6m) but not medial area 5 or lateral area 6. In a control visual-orienting task, areas 5L and 6m also yielded deficits to visual stimuli presented in the contralateral field. Thus the sound-localization deficits identified during unilateral deactivation of area 5L or 6m were not unimodal and are most likely the result of motor rather than perceptual impairments. Overall, three regions in auditory cortex (AI, PAF, AES) are critical for accurate sound localization as assessed by orienting.     

Not Just for Bimodal Neurons Anymore: The Contribution of Unimodal Neurons to Cortical Multisensory Processing

Traditionally, neuronal studies of multisensory processing proceeded by first identifying neurons that were overtly multisensory (e.g., bimodal, trimodal) and then testing them. In contrast, the present study examined, without precondition, neurons in an extrastriate visual area of the cat for their responses to separate (visual, auditory) and combined-modality (visual and auditory) stimulation. As expected, traditional bimodal forms of multisensory neurons were identified. In addition, however, many neurons that were activated only by visual stimulation (i.e., unimodal) had that response modulated by the presence of an auditory stimulus. Some unimodal neurons showed multisensory responses that were statistically different from their visual response. Other unimodal neurons had subtle multisensory effects that were detectable only at the population level. Most surprisingly, these non-bimodal neurons generated more than twice the multisensory signal in the PLLS than did the bimodal neurons. These results expand the range of multisensory convergence patterns beyond that of the bimodal neuron. However, rather than characterize a separate class of multisensory neurons, unimodal multisensory neurons may actually represent an intermediary form of multisensory convergence that exists along the functional continuum between unisensory neurons, at one end, and fully bimodal neurons at the other.     

Auditory projections to extrastriate visual cortex: connectional basis for multisensory processing in ‘unimodal’ visual neurons

Neurophysiological studies have recently documented multisensory properties in ‘unimodal’ visual neurons of the cat posterolateral lateral suprasylvian (PLLS) cortex, a retinotopically organized area involved in visual motion processing. In this extrastriate visual area, a region has been identified where both visual and auditory stimuli were independently effective in activating neurons (bimodal zone), as well as a second region where visually-evoked activity was significantly facilitated by concurrent auditory stimulation but was unaffected by auditory stimulation alone (subthreshold multisensory region). Given their different distributions, the possible corticocortical connectivity underlying these distinct forms of crossmodal convergence was examined using biotinylated dextran amine (BDA) tracer methods in 21 adult cats. The auditory cortical areas examined included the anterior auditory field (AAF), primary auditory cortex (AI), dorsal zone (DZ), secondary auditory cortex (AII), field of the rostral suprasylvian sulcus (FRS), field anterior ectosylvian sulcus (FAES) and the posterior auditory field (PAF). Of these regions, the DZ, AI, AII, and FAES were found to project to the both the bimodal zone and the subthreshold region of the PLLS. This convergence of crossmodal inputs to the PLLS suggests not only that complex auditory information has access to this region but also that these connections provide the substrate for the different forms (bimodal versus subthreshold) of multisensory processing which may facilitate its functional role in visual motion processing.     

Cortex controls multisensory depression in superior colliculus

Multisensory depression is a fundamental index of multisensory integration in superior colliculus (SC) neurons. It is initiated when one sensory stimulus (auditory) located outside its modality-specific receptive field degrades or eliminates the neuron's responses to another sensory stimulus (visual) presented within its modality-specific receptive field. The present experiments demonstrate that the capacity of SC neurons to engage in multisensory depression is strongly dependent on influences from two cortical areas (the anterior ectosylvian and rostral lateral suprasylvian sulci). When these cortices are deactivated, the ability of SC neurons to synthesize visual-auditory inputs in this way is compromised; multisensory responses are disinhibited, becoming more vigorous and in some cases indistinguishable from responses to the visual stimulus alone. Although obtaining a more robust multisensory SC response when cortex is nonfunctional than when it is functional may seem paradoxical, these data may help explain previous observations that the loss of these cortical influences permits visual orientation behavior in the presence of a normally disruptive auditory stimulus.     

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.     

Neural mechanisms for synthesizing sensory information and producing adaptive behaviors

The ability to integrate information from different sensory systems is a fundamental characteristic of the brain. Because different bits of information are derived from different sensory channels, their synthesis markedly enhances the detection and identification of external stimuli. The neural substrate for such “multisensory” integration is provided by neurons that receive convergent input from two or more sensory modalities. Many such multisensory neurons are found in the superior colliculus (SC), a midbrain structure that plays a significant role in overt attentive and orientation behaviors. The various principles governing the integration of visual, auditory, and somatosensory inputs in SC neurons have been explored in several species. Thus far, the evidence suggests a remarkable conservation of integrative features during vertebrate evolution. One of the most robust of these principles is based on spatial relationships: a striking enhancement in activity is induced in a multisensory neuron when two different sensory stimuli (e.g., visual and auditory) are in spatial concordance, whereas a profound response depression can be induced when these cues are spatially discordant. The most extensive physiological observations have been made in cat, and in this species the same principles that have been shown to govern multisensory integration at the level of the individual SC neuron have also been shown to govern overt attentive and orientation responses to multisensory stimuli. Most surprising, however, is the critical role played by association (i.e. anterior ectosylvian) cortex in facilitating these midbrain processes. In the absence of the modulating corticotectal influences, multisensory SC neurons in cat are unable to integrate the different sensory cues converging upon them in an adult-like fashion, and are unable to mediate overt multisensory behaviors. This situation appears quite similar to that observed during early postnatal life. When multisensory SC neurons first appear, they are able to respond to multiple sensory inputs but are unable to synthesize these inputs to significantly enhance or degrade their responses. During ontogeny, individual multisensory neurons develop this capacity abruptly, but at very different ages, until the mature population condition is reached after several postnatal months. It appears likely that the abrupt onset of this capacity in any individual SC neuron reflects the maturation of inputs from anterior ectosylvian cortex. Presumably, the functional coupling of cortex with an individual SC neuron is essential to initiate and maintain that neuron’s capability for multisensory integration throughout its life.     

Multisensory orientation behavior is disrupted by neonatal cortical ablation

The integration of visual and auditory information can significantly amplify the sensory responses of superior colliculus (SC) neurons and the behaviors that depend on them. This response amplification depends on the development of SC inputs that are derived from two regions of cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Neonatal ablation of these cortico-collicular areas has been shown to disrupt the development of the multisensory enhancement capabilities of SC neurons and the present results demonstrate that it also precludes the development of the normal multisensory enhancements in orientation behavior. Animals with neonatal ablation of AES and rLS were tested at maturity and found unable to benefit from the combination of visual and auditory cues in their efforts to localize targets in contralesional space. In contrast, their ipsilesional multisensory orientation capabilities were indistinguishable from those of normal animals. However, when only one of these cortical areas was removed during early life, later behavioral consequences were negligible. Whether similar compensatory processes would occur in adult animals remains to be determined. These observations, coupled with those from previous studies, also suggest that a surprisingly high proportion of SC neurons capable of multisensory integration must be present for orientation behavior benefits to be realized. Compensatory mechanisms can achieve this if early lesions spare either AES or rLS, but even the impressive plasticity of the neonatal brain cannot compensate for the early loss of both of them.     

Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat

Although the contributions of primary auditory cortex (AI) to sound localization have been extensively studied in a large number of mammals, little is known of the contributions of nonprimary auditory cortex to sound localization. Therefore the purpose of this study was to examine the contributions of both primary and all the recognized regions of acoustically responsive nonprimary auditory cortex to sound localization during both bilateral and unilateral reversible deactivation. The cats learned to make an orienting response (head movement and approach) to a 100-ms broad-band noise stimulus emitted from a central speaker or one of 12 peripheral sites (located in front of the animal, from left 90 degrees to right 90 degrees , at 15 degrees intervals) along the horizontal plane after attending to a central visual stimulus. Twenty-one cats had one or two bilateral pairs of cryoloops chronically implanted over one of ten regions of auditory cortex. We examined AI [which included the dorsal zone (DZ)], the three other tonotopic fields [anterior auditory field (AAF), posterior auditory field (PAF), ventral posterior auditory field (VPAF)], as well as six nontonotopic regions that included second auditory cortex (AII), the anterior ectosylvian sulcus (AES), the insular (IN) region, the temporal (T) region [which included the ventral auditory field (VAF)], the dorsal posterior ectosylvian (dPE) gyrus [which included the intermediate posterior ectosylvian (iPE) gyrus], and the ventral posterior ectosylvian (vPE) gyrus. In accord with earlier studies, unilateral deactivation of AI/DZ caused sound localization deficits in the contralateral field. Bilateral deactivation of AI/DZ resulted in bilateral sound localization deficits throughout the 180 degrees field examined. Of the three other tonotopically organized fields, only deactivation of PAF resulted in sound localization deficits. These deficits were virtually identical to the unilateral and bilateral deactivation results obtained during AI/DZ deactivation. Of the six nontonotopic regions examined, only deactivation of AES resulted in sound localization deficits in the contralateral hemifield during unilateral deactivation. Although bilateral deactivation of AI/DZ, PAF, or AES resulted in profound sound localization deficits throughout the entire field, the cats were generally able to orient toward the hemifield that contained the acoustic stimulus, but not accurately identify the location of the stimulus. Neither unilateral nor bilateral deactivation of areas AAF, VPAF, AII, IN, T, dPE, nor vPE had any effect on the sound localization task. Finally, bilateral heterotopic deactivations of AI/DZ, PAF, or AES yielded deficits that were as profound as bilateral homotopic cooling of any of these sites. The fact that deactivation of any one region (AI/DZ, PAF, or AES) was sufficient to produce a deficit indicated that normal function of all three regions was necessary for normal sound localization. Neither unilateral nor bilateral deactivation of AI/DZ, PAF, or AES affected the accurate localization of a visual target. The results suggest that hemispheric deactivations contribute independently to sound localization deficits.     

Nonequivalent visual, auditory, and somatic corticotectal influences in cat

1. The effects of cortical cooling on the responses of cells to visual, somatic, and acoustic stimuli were studied in the cat superior colliculus (SC). When the visual cortex was cooled, the responses of many visual cells of the SC were depressed or eliminated, but the activity of nonvisual cells remained unchanged. This response depression was found in visual cells located in both superficial and deep laminae and was most pronounced in neurons which were binocular and directionally selective. 2. Cooling somatic and/or auditory cortex had no effect on visual SC cells and, with few exceptions, did not alter the activity of somatic or acoustic cells either. 3. The specificity of visual cortex influences on visual responding in the SC was most apparent in multimodal cells. In trimodal cells, the simultaneous cooling of visual, somatic, and auditory cortex eliminated responses to visual stimuli, but did not affect responses to somatic or acoustic stimuli. Visual responses were returned to the precooling level in both unimodal and multimodal cells by cortical rewarming. 4. The present experiments indicate that despite the organizational parallels among visual, somatic, and acoustic cells of the cat SC, the influences they receive from cortex are non-equivalent. Cortical influences appear to play a more critical role in the responses of visual cells than in the responses of somatic and acoustic cells. These observations raise questions about the functional significance of nonvisual corticotectal systems.     

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.     

Multisensory processing via early cortical stages: Connections of the primary auditory cortical field with other sensory systems

It is still a popular view that primary sensory cortices are unimodal, but recent physiological studies have shown that under certain behavioral conditions primary sensory cortices can also be activated by multiple other modalities. Here, we investigate the anatomical substrate, which may underlie multisensory processes at the level of the primary auditory cortex (field AI), and which may, in turn, enable AI to influence other sensory systems. We approached this issue by means of the axonal transport of the sensitive bidirectional neuronal tracer fluorescein-labeled dextran which was injected into AI of Mongolian gerbils (Meriones unguiculatus). Of the total number of retrogradely labeled cell bodies (i.e. cells of origin of direct projections to AI) found in non-auditory sensory and multisensory brain areas, approximately 40% were in cortical areas and 60% in subcortical structures. Of the cell bodies in the cortical areas about 82% were located in multisensory cortex, viz., the dorsoposterior and ventroposterior, posterior parietal cortex, the claustrum, and the endopiriform nucleus, 10% were located in the primary somatosensory cortex (hindlimb and trunk region), and 8% in secondary visual cortex. The cortical regions with retrogradely labeled cells also contained anterogradely labeled axons and their terminations, i.e. they are also target areas of direct projections from AI. In addition, the primary olfactory cortex was identified as a target area of projections from AI. The laminar pattern of corticocortical connections suggests that AI receives primarily cortical feedback-type inputs and projects in a feedforward manner to its target areas. Of the labeled cell bodies in the subcortical structures, approximately 90% were located in multisensory thalamic, 4% in visual thalamic, and 6% in multisensory lower brainstem structures. At subcortical levels, we observed a similar correspondence of retrogradely labeled cells and anterogradely labeled axons and terminals in visual (posterior limitans thalamic nucleus) and multisensory thalamic nuclei (dorsal and medial division of the medial geniculate body, suprageniculate nucleus, posterior thalamic cell group, zona incerta), and in the multisensory nucleus of the brachium of the inferior colliculus. Retrograde, but not anterograde, labeling was found in the multisensory pontine reticular formation, particularly in the reticulotegmental nucleus of the pons. Conversely, anterograde, but no retrograde, labeling was found in the visual laterodorsal and lateroposterior thalamic nuclei, in the multisensory peripeduncular, posterior intralaminar, and reticular thalamic nuclei, as well as in the multisensory superior and pericentral inferior colliculi (including cuneiform and sagulum nucleus), pontine nuclei, and periaqueductal gray. Our study supports the notion that AI is not merely involved in the analysis of auditory stimulus properties but also in processing of other sensory and multisensory information. Since AI is directly connected to other primary sensory cortices (viz. the somatosensory and olfactory ones) multisensory information is probably also processed in these cortices. This suggests more generally, that primary sensory cortices may not be unimodal.     

Visual, auditory, and somatosensory convergence on cells in superior colliculus results in multisensory integration

Convergence of inputs from different sensory modalities onto individual neurons is a phenomenon that occurs widely throughout the brain at many phyletic levels and appears to represent a basic neural mechanism by which an organism integrates complex environmental stimuli. In the present study, neurons in the superior colliculus (SC) were used as a model to examine how single neurons deal with simultaneous cues from different sensory modalities (e.g., visual, auditory, somatosensory). The functional result of multisensory convergence on an individual cell was determined by comparing the responses evoked from it by a combined-modality (multimodal) stimulus with those elicited by each (unimodal) component of that stimulus presented alone. Superior colliculus cells exhibited profound changes in their activity when individual sensory stimuli were combined. These "multisensory interactions" were found to be widespread among deep laminae cells and fell into one of two functional categories: response enhancement, characterized by a significant increase in the number of discharges evoked; and response depression, characterized by a significant decrease in the discharges elicited. Multisensory response interactions most often reflected a multiplicative, rather than summative, change in activity. Their absolute magnitude varied from cell to cell and, when stimulus conditions were altered, within the same cell. However, the percentage change of enhanced interactions was generally inversely related to the vigor of the responses that could be evoked by presenting each unimodal stimulus alone and suggest that the potential for response amplification was greatest when responses evoked by individual stimuli were weakest. The majority of cells exhibiting multi-sensory characteristics were demonstrated to have descending efferent projections and thus had access to premotor and motor areas of the brain stem and spinal cord involved in SC-mediated attentive and orientation behaviors. These data show that multisensory convergence provides the descending efferent cells of the SC with a dynamic response character. The responses of these cells and the SC-mediated behaviors that they underlie need not be immutably tied to the presence of any single stimulus, but can vary in response to the particular complex of stimuli present in the environment at any given moment.     

Competition and convergence between auditory and cross-modal visual inputs to primary auditory cortical areas

Sensory neocortex is capable of considerable plasticity after sensory deprivation or damage to input pathways, especially early in development. Although plasticity can often be restorative, sometimes novel, ectopic inputs invade the affected cortical area. Invading inputs from other sensory modalities may compromise the original function or even take over, imposing a new function and preventing recovery. Using ferrets whose retinal axons were rerouted into auditory thalamus at birth, we were able to examine the effect of varying the degree of ectopic, cross-modal input on reorganization of developing auditory cortex. In particular, we assayed whether the invading visual inputs and the existing auditory inputs competed for or shared postsynaptic targets and whether the convergence of input modalities would induce multisensory processing. We demonstrate that although the cross-modal inputs create new visual neurons in auditory cortex, some auditory processing remains. The degree of damage to auditory input to the medial geniculate nucleus was directly related to the proportion of visual neurons in auditory cortex, suggesting that the visual and residual auditory inputs compete for cortical territory. Visual neurons were not segregated from auditory neurons but shared target space even on individual target cells, substantially increasing the proportion of multisensory neurons. Thus spatial convergence of visual and auditory input modalities may be sufficient to expand multisensory representations. Together these findings argue that early, patterned visual activity does not drive segregation of visual and auditory afferents and suggest that auditory function might be compromised by converging visual inputs. These results indicate possible ways in which multisensory cortical areas may form during development and evolution. They also suggest that rehabilitative strategies designed to promote recovery of function after sensory deprivation or damage need to take into account that sensory cortex may become substantially more multisensory after alteration of its input during development.     

Neonatal cortical ablation disrupts multisensory development in superior colliculus

The ability of cat superior colliculus (SC) neurons to synthesize information from different senses depends on influences from two areas of the cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Reversibly deactivating the inputs to the SC from either of these areas in normal adults severely compromises this ability and the SC-mediated behaviors that depend on it. In this study, we found that removal of these areas in neonatal animals precluded the normal development of multisensory SC processes. At maturity there was a substantial decrease in the incidence of multisensory neurons, and those multisensory neurons that did develop were highly abnormal. Their cross-modal receptive field register was severely compromised, as was their ability to integrate cross-modal stimuli. Apparently, despite the impressive plasticity of the neonatal brain, it cannot compensate for the early loss of these cortices. Surprisingly, however, neonatal removal of either AES or rLS had comparatively minor consequences on these properties. At maturity multisensory SC neurons were quite common: they developed the characteristic spatial register among their unisensory receptive fields and exhibited normal adult-like multisensory integration. These observations suggest that during early ontogeny, when the multisensory properties of SC neurons are being crafted, AES and rLS may have the ability to compensate for the loss of one another's cortico-collicular influences so that normal multisensory processes can develop in the SC.     

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. Electronic Publication     

Restoration of acoustic orienting into a cortically deaf hemifield by reversible deactivation of the contralesional superior colliculus: the acoustic "Sprague Effect"

Removal of all contiguous visual cortical areas of one hemisphere results in a contralateral hemianopia. Subsequent deactivation of the contralesional superior colliculus (SC) nullifies the effects of the visual cortex ablation and restores visual orienting responses into the cortically blind hemifield. This deficit nullification has become known as the "Sprague Effect." Similarly, in the auditory system, unilateral ablation of auditory cortex results in severe sound localization deficits, as assessed by acoustic orienting, to stimuli in the contralateral hemifield. The purpose of this study was to examine whether auditory orienting responses can be restored into the impaired hemifield during deactivation of the contralesional SC. Three mature cats were trained to orient toward and approach an acoustic stimulus (broadband, white noise burst) that was presented centrally, or at one of 12 peripheral loci, spaced at 15 degrees intervals. After training, a cryoloop was chronically implanted over the dorsal surface of the right SC. During cooling of the cooling loop to temperatures sufficient to deactivate the superficial and intermediate layers (SZ, SGS, SO, SGI), auditory orienting responses were eliminated into the left (contracooled) hemifield while leaving acoustic orienting into the right (ipsicooled) hemifield unimpaired. This deficit was temperature-dependently graded from periphery to center. After the effectiveness of the SC cooling loop was verified, auditory cortex of the middle and posterior ectosylvian and anterior and posterior sylvian gyri was removed from the left hemisphere. As expected, the auditory cortex ablation resulted in a profound deficit in orienting to acoustic stimuli presented at any position in the right (contralesional) hemifield, while leaving acoustic orienting into the left (ipsilesional) hemifield unimpaired. The ablations of auditory cortex did not have any impact on a visual detection and orienting task. The additional deactivation of the contralesional SC to temperatures sufficient to cool the superficial and intermediate layers nullified the deficit caused by the auditory cortex ablation and acoustic orienting responses were restored into the right hemifield. This restoration was temperature-dependently graded from center to periphery. The deactivations were localized and confirmed with reduced uptake of radiolabeled 2-deoxyglucose. Therefore deactivation of the right superior colliculus after the ablation of the left auditory cortex yields a fundamentally different result from that identified during deactivation of the right superior colliculus before the removal of left auditory cortex in the same animal. Thus the "Sprague Effect" is not unique to a particular sensory system and deactivation of the contralesional SC can restore either visual or acoustic orienting responses into an impaired hemifield after cortical damage.     

Topographic organization of somatosensory corticotectal influences in cat

Using electrophysiological techniques, the present study demonstrated that substantial direct somatosensory cortical influences on the superior colliculus (SC) originate from three areas: a) SIV, b) para-SIV (the cortex adjacent to SIV but deeper in the anterior ectosylvian sulcus (AES) and for which no topography has yet been described), and c) the rostral suprasylvian sulcus. Influences also appeared to originate from SI and SII, but these may have been indirect. Detailed examination of the AES revealed that these corticotectal projections are topographically organized, and stimulation of a given cortical locus was observed to affect only those cells in the SC whose receptive fields overlapped those of cells at the stimulation site. A similar receptive-field register was found between the suprasylvian sulcus and the SC. Within this topographic pattern, considerable convergence was evident and an individual SC cell could be influenced from a surprisingly large cortical area. This was particularly evident within the representation of the forelimb. Thus, an SC cell with a receptive field covering the forelimb and paw could receive convergent input from many cortical cells with receptive fields covering all or restricted portions of this body region. Considerable corticotectal divergence also was observed within this general topographic scheme. For example, a given corticotectal site representing the digits sent projections to many different SC cells that included the digits within their receptive fields. These data are more consistent with a block-to-block than a point-to-point corticotectal projection. Somatosensory corticotectal projections excited only those SC cells that could also be activated by peripheral somatosensory stimuli. Similarly, the caudal AES, which contains auditory cells, excited only those SC cells activated also by peripheral auditory stimuli. Yet convergent influences from both auditory and somatosensory regions of the AES were observed in the SC cells that could be activated by both auditory and somatosensory stimuli. These data indicate that the AES is a major source of excitatory input to cells of the deep laminae of the SC. Since it is these deep laminae cells that project to premotor regions of the brain stem and the spinal cord, it is reasonable to suppose that the AES has a significant impact on the output signals of the SC that initiate the orientation responses to peripheral sensory stimulation.     

Effects of cooling somatosensory cortex on response properties of tactile cells in the superior colliculus

The corticotectal influences of somatosensory cortex were investigated by using reversible deactivation of cortex by cooling. More than half of the somatosensory superior colliculus (SC) cells studied exhibited a response depression (often not apparent qualitatively) or an elimination of responses to somatosensory stimuli during the period in which cortex was rendered inactive. Responses were restored to their initial levels by cortical rewarming. Hyperresponsiveness was never observed as a consequence of cortical cooling. Susceptibility to cooling-induced depression was not invariably linked to a specific cell type, location in the SC, or receptive-field size. Yet cells that had small receptive fields and were activated by hair displacement had the highest probability of being affected by this procedure. In some cells a contraction of the receptive field was induced by cortical cooling. This observation is consistent with previous experiments that showed that SC somatosensory receptive fields are constructed by the convergence of ascending and descending inputs and indicates that the responsiveness of specific receptive-field regions may depend on the functional integrity of cortex. Two cortical regions were found to produce cooling-induced effects in somatosensory SC cells: 1) SIV (and para-SIV), located in the anterior ectosylvian sulcus, and 2) the cortex within the rostral suprasylvian sulcus. These results indicate that somatosensory cortex, like visual cortex, plays a critical role in modulating the responses of SC cells. Apparently, the ability of both somatosensory and visual SC cells to code the presence of peripheral stimuli depends largely on the functional influences of their respective cortices. However, in contrast to previous observations on visual corticotectal influences, no specific receptive-field properties could be shown to be impressed on SC cells by somatosensory cortex.