Spatial Heterogeneity of Cortical Receptive Fields and Its Impact on Multisensory Interactions

Abstract

Carriere BN, Royal DW, Wallace MT. Spatial heterogeneity of cortical receptive fields and its impact on multisensory interactions. J Neurophysiol 99: 2357-2368, 2008. First published February 20, 2008 doi:10.1152/jn.01386.2007. Investigations of multisensory processing at the level of the single neuron have illustrated the importance of the spatial and temporal relationship of the paired stimuli and their relative effectiveness in determining the product of the resultant interaction. Although these principles provide a good first-order description of the interactive process, they were derived by treating space, time, and effectiveness as independent factors. In the anterior ectosylvian sulcus (AES) of the cat, previous work hinted that the spatial receptive field (SRF) architecture of multisensory neurons might play an important role in multisensory processing due to differences in the vigor of responses to identical stimuli placed at different locations within the SRF. In this study the impact of SRF architecture on cortical multisensory processing was investigated using semichronic single-unit electrophysiological experiments targeting a multisensory domain of the cat AES. The visual and auditory SRFs of AES multisensory neurons exhibited striking response heterogeneity, with SRF architecture appearing to play a major role in the multisensory interactions. The deterministic role of SRF architecture was tightly coupled to the manner in which stimulus location modulated the responsiveness of the neuron. Thus multisensory stimulus combinations at weakly effective locations within the SRF resulted in large (often superadditive) response enhancements, whereas combinations at more effective spatial locations resulted in smaller (additive/subadditive) interactions. These results provide important insights into the spatial organization and processing capabilities of cortical multisensory neurons, features that may provide important clues as to the functional roles played by this area in spatially directed perceptual processes.

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

“…Finally, cross-sensory modulations may target subsets of neurons based on their response level, laminar location, and neuron type within each rearing condition. The fact that the auditory clicks failed to drive any barrel cortex neurons under any conditions in the present study indicates that the cross-sensory multisensory interactions observed here are modulatory in nature (Dehner et al, 2004;Lakatos et al, 2007;Carriere et al, 2008), as opposed to the directly driven responses found in association cortex (Wallace et al, 1992;Carriere et al, 2007), and may account for the difficulty in detecting multisensory influences in primary sensory cortex. Surprisingly, the modulatory influence is present even in normally reared rats and is maximally enhanced when whisker deprivation is coupled with click rearing.…”

Looming Signals Reveal Synergistic Principles of Multisensory Integration

“…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. 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).…”

“…Parallel evidence at the single-neuron level similarly nuances how principles of multisensory interactions cooperate. Responses expressing multisensory interactions within subregions of a neuron's receptive field are heterogeneous and give rise to integrative "hot spots" (Carriere et al, 2008).…”

Bridging the gap: Synaesthesia and multisensory processes

“…Recent strides within this area have extended our understanding of the neural correlates of multisensory integration from the single cell to more distributed neural representations, have begun to provide evidence on the role of dynamic binding mechanisms in multisensory processing (e.g. Cappe et al, 2009Cappe et al, , 2012Carriere et al, 2008;Maier et al, 2008;Royal et al, 2009;Senkowski et al, 2007) and started to establish strong functional links between neural activity profiles and changes in behavior and perception (e.g. Murray et al, 2016).…”