Visual Deprivation Alters the Development of Cortical Multisensory Integration

Abstract

It has recently been demonstrated that the maturation of normal multisensory circuits in the cortex of the cat takes place over an extended period of postnatal life. Such a finding suggests that the sensory experiences received during this time may play an important role in this developmental process. To test the necessity of sensory experience for normal cortical multisensory development, cats were raised in the absence of visual experience from birth until adulthood, effectively precluding all visual and visual-nonvisual multisensory experiences. As adults, semichronic single-unit recording experiments targeting the anterior ectosylvian sulcus (AES), a well-defined multisensory cortical area in the cat, were initiated and continued at weekly intervals in anesthetized animals. Despite having very little impact on the overall sensory representations in AES, dark-rearing had a substantial impact on the integrative capabilities of multisensory AES neurons. A significant increase was seen in the proportion of multisensory neurons that were modulated by, rather than driven by, a second sensory modality. More important, perhaps, there was a dramatic shift in the percentage of these modulated neurons in which the pairing of weakly effective and spatially and temporally coincident stimuli resulted in response depressions. In normally reared animals such combinations typically give rise to robust response enhancements. These results illustrate the important role sensory experience plays in shaping the development of mature multisensory cortical circuits and suggest that dark-rearing shifts the relative balance of excitation and inhibition in these circuits.

Crossmodal reorganization in the early deaf switches sensory, but not behavioral roles of auditory cortex

“…1, revealed physiologically active neurons (n = 415), the majority of which (67.7% ± 7.6 SD) were responsive to visual stimulation. By contrast, similar recordings from the FAES in adult hearing cats (n = 3) in this and in previous studies (2,22,23,(25)(26)(27)(28) showed a strong preference auditory responsivity, although a small proportion of nonauditory responses also occurred (Fig. 1).…”

“…What is known of the FAES suggests that unmasking may have at least a partial role in its reorganization following deafness. In hearing animals, ∼30% of FAES neurons show modulation of auditory responses by activation of an adjacent somatosensory area (24), and ∼30% of neurons can be influenced by visual stimulation (23,27). Therefore, with a reduction of auditory inputs after deafness, it would be expected that existing nonauditory inputs to the FAES would be unmasked.…”

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.…”

Multisensory integration and neuroplasticity in the human cerebral cortex

“…The same seems to be true for subcortical multisensory regions such as in the superior colliculus [69]. Similar results have been obtained in human infants that show age-dependent effects on reaction times when tested in localization of auditory, visual or audiovisual stimuli [70]. Nevertheless, some basic multisensory processes seem to be in place quite early in human life as indicated by data from 5-month-old infants regarding the discrimination of visual, auditory or audiovisual rhythms [71] and processing of audiovisual correspondences between the height of a pitch and the height of a visual stimulus [56].…”