Barry E. Stein will introduce the issues by briefly describing an early plasticity and compensatory mechanism that is restricted to the various sensory-specific components of the cortico-collicular pathway, a pathway that is critical for multisensory integration in the superior colliculus (SC), as well as for SC-mediated attentive, orientation and localization function.
Terrence R. Stanford will discuss the nature of the influence of this cortico-collicular pathway by detailing how its components operate, and by identifying a crucial synergy among them. This synergy must be expressed for the cortico-collicular projection to facilitate mulitsensory integration in its target SC neurons.
Benjamin Rowland will present data indicating that the functional plasticity in this system is not restricted to early life. Under the proper circumstance adult experience with cross-modal cues can compensate for early deprivation at the neuronal and behavioral levels. He will discuss how these findings in animal models might explain human subject performance on multisensory tasks after early sensory dysfunctions are corrected later in life (e.g., surgical removal of congenital cataracts, hearing aids or cochlear implants).
John G. McHaffie will also deal with adult plasticity in multisensory integration. He will show how cross-modal cues can be used in a behavioral training paradigm to ameliorate the visual hemineglect induced by unilateral removal of all contiguous visual cortices in adult animals, the physiological changes that occurs in the superior colliculus multisensory neurons as a consequence of this cross-modal training, and the dependence of these behaviorally-induced changes on multisensory regions of cortex.
Elisabetta Ladavas will show how this multisensory integration strategy has proved effective in the rehabilitation of patients with stroke-induced hemianopia, and its possible applicability to other patient populations.
Abstracts:
Developmental Plasticity in the Cortical Control of Multisensory Integration in the Superior Colliculus: Barry E. Stein
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 in individual neurons and the SC-mediated behaviors that depend on it. In the current studies 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. Similarly, the SC-mediated behaviors dependent on this capacity were also eliminated. 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 either the single neuron or behavioral levels. 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. Similarly, animals showed the characteristic benefit to multisensory integration in initiating and guiding orientation and approach behaviors. 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. Whether similar compensatory processes could be initiated in adult animals remains to be determined. Supported by NIH grants EY016716 and NS 36916.

Multisensory Integration in the Superior Colliculus Requires Synergy among Cortical Inputs from Modality-Specific Subregions of the Anterior Ectosylvian Sulcus: Terrence R. Stanford
Influences from the visual (AEV), auditory (FAES) and somatosensory (SIV) divisions of the cat anterior ectosylvian sulcus (AES) play a critical role in rendering superior colliculus (SC) neurons capable of multisensory integration. However, it is not known if this is accomplished via their independent sensory-specific actions or via some cross-modal cooperative action that emerges as a consequence of their convergence on SC neurons. Using visual-auditory SC neurons as a model, we examined how selective and combined deactivation of FAES and AEV affected SC multisensory (visual-auditory) and unisensory (visual-visual) integrative capabilities. Cryogenic deactivation of either FAES or AEV eliminated the multisensory response enhancement that is characteristic for SC neurons, an effect that was only marginally greater when both were deactivated simultaneously. These results indicate that SC multisensory integration  depends  on the cooperative action of distinct subsets of unisensory corticofugal afferents; afferents whose sensory combination matches the multisensory profile of their midbrain target neurons, and whose functional synergy is specific to rendering SC neurons capable of synthesizing information from those particular senses. Supported by NIH grants EY016716 and NS 36916.

Long-term Plasticity in SC Multisensory Integration: the Acquisition of Multisensory Integration Capabilities During Adulthood: Benjamin Rowland
It has been shown that the ability of neurons in the superior colliculus (SC) to integrate information across sensory modalities depends on inputs from unisensory neurons in specific regions of association cortex (i.e., the anterior ectosylvian sulcus and rostral lateral suprasylvian sulcus in the cat). Temporary deactivation of these regions unilaterally during a circumscribed developmental window (using slow-release Elvax-muscimol implants) precluded the normal development of multisensory integration in SC neurons and their associated behaviors (localization/orientation) in the affected hemifield when assessed at 1 year of age. These deficits were therefore long-lasting and appeared permanent. However, when animals were later examined at 5 years of age, multisensory enhancements were evident in behavior on both sides of space. Physiological examinations revealed that, in the same animals, SC neurons on both sides of space showed multisensory enhancement in their responses to coincident cross-modal stimuli: multisensory responses contained more impulses and had shorter latencies than the responses to the most effective of these modality-specific component stimuli. These data suggest that 1) specific regions of association cortex are the vehicle through which multisensory integration in the SC develops postnatally, 2) early interventions that deactivate these regions during circumscribed windows of time yield long-lasting and substantial deficits in multisensory integration in the SC, 3) However, plasticity in the development of SC multisensory integration is not limited to a circumscribed period of the first few months of postnatal life: the capacity to develop multisensory integration is also present in the adult, and although its time course appears far more protracted, its potency once developed is no less robust. Supported by NIH grants EY016716 and NS 36916.

Cross-modal Rehabilitative Training Ameliorates Visuomotor Deficits Produced by Visual Cortex Lesions: John G. McHaffie
The superior colliculus (SC) requires influences from visual cortex to play its critical role in mediating contralateral visual orientation: unilateral visual cortex lesions eliminate this capacity and induce an enduring contralateral hemineglect. Given that auditory cues can have a profound influence on visual processing in certain behavioral circumstances, we posited that multisensory cortical regions might be recruited to compensate, in part, for the lost visual cortex. We tested this possibility with a rehabilitative strategy involving a cross-modal training paradigm. Cats with lesion-induced visual hemineglect were trained to orient to spatially and temporally coincident multisensory (auditory-visual) cues in the neglected hemifield. After one month of training, the cats had permanently regained the ability to orient to visual cues in the previously neglected hemifield whereas their untrained counterparts did not. Subsequent removal of ipsilesional anterior ectosylvian sulcus (AES) eliminated this reinstated visuomotor capacity, despite the fact that AES lesions normally have no effect on visual orientation behaviors. Presumably, repetitive orientation elicited by the auditory component of the cross-modal cue induced use-dependent alterations in the remaining neural architecture that ultimately re-established associations between visual cues and motor acts. Electrophysiological data suggested a neural correlate of this behavioral recovery: after cross-modal training, ipsilesional SC neurons regained robust visual responsiveness that had been lost following visual cortex lesions. Taken together, these data suggest that a functionally remodeled cortico-collicular circuit emerges as a consequence of cross-modal training that can compensate for the deleterious behavioral and physiological effects of visual cortex lesions. Supported by NIH grant NS35008.

A Multisensory-based Approach to the Recovery of a Unisensory Deficit:
Elisabetta Làdavas
The human brain is provided with a flexible audio-visual system. This system interprets and guides responses to external events according to the spatial alignment, temporal synchronization and effectiveness of modality-specific signals. Here I will explore the possibility that such a system might represent the neural correlate of sensory compensation after damage to one sensory pathway. This hypothesis will be developed by considering results from behavioural studies in which spatial information from one sensory modality has been rendered weakly effective (healthy subjects) or damaged by a cerebral lesion (patients with visual field defect or visual neglect). In the first part, I will discuss evidence for the pivotal role of the superior colliculus-extrastriate pathway in responding to cross-modal stimulation when an overt orienting response is required. In the second part, I will examine the relevance of this pathway for the short and long-term effects of audio-visual stimulation on the visual and spatial impairments following damage to the geniculo-striate pathway.