Spatial receptive field organization of multisensory neurons and its impact on multisensory interactions

Abstract

Previous work has established that the spatial receptive fields (SRFs) of multisensory neurons in the cerebral cortex are strikingly heterogeneous, and that SRF architecture plays an important deterministic role in sensory responsiveness and multisensory integrative capacities. The initial part of this contribution serves to review these findings detailing the key features of SRF organization in cortical multisensory populations by highlighting work from the cat anterior ectosylvian sulcus (AES). In addition, we have recently conducted parallel studies designed to examine SRF architecture in the classic model for multisensory studies, the cat superior colliculus (SC), and we present some of the preliminary observations from the SC here. An examination of individual SC neurons revealed marked similarities between their unisensory (i.e., visual and auditory) SRFs, as well as between these unisensory SRFs and the multisensory SRF. Despite these similarities within individual neurons, different SC neurons had SRFs that ranged from a single area of greatest activation (hot spot) to multiple and spatially discrete hot spots. Similar to cortical multisensory neurons, the interactive profile of SC neurons was correlated strongly to SRF architecture, closely following the principle of inverse effectiveness. Thus, large and often superadditive multisensory response enhancements were typically seen at SRF locations where visual and auditory stimuli were weakly effective. Conversely, subadditive interactions were seen at SRF locations where stimuli were highly effective. Despite the unique functions characteristic of cortical and subcortical multisensory circuits, our results suggest a strong mechanistic interrelationship between SRF microarchitecture and integrative capacity. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. NIH Public Access An introduction to multisensory interactionsOur environment is comprised of myriad sensory cues that are constantly changing along numerous dimensions (e.g., space, effectiveness, etc.). As a consequence of the dynamic nature of our sensory world, the nervous system is continually challenged with resolving the inherent ambiguities that result from these competing stimulus complexes in order to generate directed action and create veridical percepts. To accomplish this task, the brain has to correctly identify whether sensory energies propagated in different domains (e.g., light, sound, etc.) belong to a single event or are derived from several discrete events. Specialized structures, including the midbrain superior colliculus (SC), have e...

Looming Signals Reveal Synergistic Principles of Multisensory Integration

“…The present observation of selective superadditive interactions of responses to multisensory looming signals during early poststimulus onset periods (73-113 ms) that were moreover positively correlated with behavioral facilitation argues for synergistic interplay in humans between principles of multisensory integration established from single-neuron recordings in animals (Stein and Meredith, 1993). These results, in conjunction with the extant literature, highlight the challenge of directly transposing models of multisensory interactions from single-neuron to populationlevel responses and perception (Krueger et al, 2009;Ohshiro et al, 2011). They likewise suggest that multisensory interactions can facilitate the processing and perception of specific varieties of ethologically significant environmental stimuli; here those signaling potential collisions/dangers.…”

“…Superadditive and subadditive hotspots are not stationary within the neuron's receptive field either in cortical (Carriere et al, 2008) or subcortical ) structures and furthermore are not straightforwardly predicted by unisensory response patterns. These features were further evident when data were analyzed at a population level, such that the percentage of integration was higher (in their population of neurons) along the horizontal meridian than for other positions, even though response profiles were uniformly distributed (Krueger et al, 2009). Regarding potential functional consequences of this organization of responsiveness, Wallace and colleagues postulate that such heterogeneity could be efficient in encoding dynamic/moving stimuli and in generating a "normalized" response profile (at least during multisensory conditions) across the receptive field (Krueger et al, 2009).…”

“…These features were further evident when data were analyzed at a population level, such that the percentage of integration was higher (in their population of neurons) along the horizontal meridian than for other positions, even though response profiles were uniformly distributed (Krueger et al, 2009). Regarding potential functional consequences of this organization of responsiveness, Wallace and colleagues postulate that such heterogeneity could be efficient in encoding dynamic/moving stimuli and in generating a "normalized" response profile (at least during multisensory conditions) across the receptive field (Krueger et al, 2009). The present results may be highlighting the consequences of such architecture (to the extent it manifests in humans) on the discrimination and population-level neural response to dynamic looming stimuli.…”

“…In agreement, the extant literature in humans provides several replications from independent laboratories of early-latency (i.e., Ͻ100 ms poststimulus onset) nonlinear neural response interactions between high-intensity auditory-visual stimulus pairs (Giard and Peronnet, 1999 Evidence for synergy between principles of multisensory interactions is likewise accumulating in studies of single-unit spiking activity within the cat anterior ectosylvian sulcus. The innovative discovery is that the firing rate within individual receptive fields of neurons is heterogeneous and varies with stimulus effectiveness in spatially and temporally dependent manners (for review, see Krueger et al, 2009). Superadditive and subadditive hotspots are not stationary within the neuron's receptive field either in cortical (Carriere et al, 2008) or subcortical ) structures and furthermore are not straightforwardly predicted by unisensory response patterns.…”

Developmental plasticity of multisensory circuitry: how early experience dictates cross-modal interactions

“…Given that random exposure to audiovisual stimuli precludes establishing relationships between stimuli that should or should not be bound together, and that response depressions generally occur for stimuli encoded as separate events [e.g., auditory and visual stimuli presented from distinct spatial locations and therefore likely belonging to independent sources (Meredith and Stein 1996)], it is possible that the incidence of response depressions would also decrease in the random exposure group due to increased inexperience with statistically meaningful relationships between audiovisual events. Recent studies have also shown that the receptive fields of multisensory SC neurons are heterogeneous (Krueger et al 2009) and that neuronal responsiveness and integrative abilities of the same neuron change with the spatial location being tested within the receptive field. Thus, it would be interesting to present stimuli at different, but controlled, receptive field locations (such as within or outside of "hotspots"; see Fig.…”