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

Abstract

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.

Heterogeneity in the spatial receptive field architecture of multisensory neurons of the superior colliculus and its effects on multisensory integration

“…A detailed mapping of each of the SRFs (i.e., visual, auditory and visual-auditory) was possible for 64 of these neurons, which often entailed isolation of the neuron for periods of several hours. In accordance with the previous literature (Meredith and Stein, 1983, Stein BE 1993, Kadunce et al, 2001; Meredith and Stein 1996;Meredith and Stein 1986; Meredith and Stein 1990; Stein BE 1993), the majority of these multisensory neurons demonstrated considerable overlap in the spatial extent of their visual and auditory receptive fields.…”

Development of multisensory integration from the perspective of the individual neuron

“…Superior colliculus neurons trained with spatially and temporally concordant visual–auditory stimuli exhibit preferences for a cross-modal stimulus with that configuration. Their responses are progressively degraded as the component stimuli are separated from one another in space and/or time, a systematic bias that is not evident in normal animals 81,82 . Multisensory response magnitude in normal animals has no systematic relationship with the location of the visual and auditory stimuli within their overlapping receptive fields, and these neurons prefer that the visual stimulus precede the auditory by 50–100 ms.…”

“…The first two involve space and time. Cross-modal (for example, visual–auditory) cues that are in close spatial and temporal register generally enhance the responses of multisensory neurons, whereas those that are spatially or temporally disparate often elicit response depression or fail to be integrated 81,82 . The third principle, that of ‘inverse effectiveness’ (REF.…”

Stimulus intensity modulates multisensory temporal processing

“…Although these studies have illustrated the central importance of time in dictating human multisensory interactions, other studies have focused on the roles of space (Bertelson & Radeau, 1981; Ghose & Wallace, 2014; Kadunce, Vaughan, Wallace, & Stein, 2001; Krueger, Royal, Fister, & Wallace, 2009; Macaluso, et al, 2004; Mahoney, et al, 2015; Meredith & Stein, 1986, 1996; Radeau & Bertelson, 1974; Royal, Carriere, & Wallace, 2009; Royal, Krueger, Fister, & Wallace, 2010; Sarko, et al, 2012; Vroomen, Bertelson, & de Gelder, 2001; Wallace, et al., 2004) and effectiveness (James & Stevenson, 2012a; James, et al., 2012; Kim & James, 2010; Kim, Stevenson, & James, 2012; Leone & McCourt, 2013; Liu, Lin, Gao, & Dang, 2013; Nath & Beauchamp, 2011; Stevenson & James, 2009; Werner & Noppeney, 2010; Yalachkov, Kaiser, Doehrmann, & Naumer, 2015). Collectively, we have learned a great deal from these studies about how stimulus-related factors shape the multisensory process, but most have treated time, space and effectiveness as independent contributors to the final multisensory product.…”