The role of sensory experience in multisensory development

The protracted timeline over which multisensory processes develop suggests that sensory experience may play an integral role in the shaping of the final functional state of these circuits. To test this hypothesis, our laboratory has carried out experiments in which early sensory experiences are altered, and then examined the consequent impact on multisensory neurons and their integrative characteristics. In the first of these experiments, cats were raised in an environment devoid of visual experience from birth until adulthood, hence abolishing the animal’s experience with associating visual and non-visual cues. Somewhat surprisingly, when examined as adults, these animals were found to have a fairly normal complement of multisensory neurons in both subcortical (i.e. SC) and cortical multisensory structures, which included a substantial population of visually responsive multisensory neurons (Carriere et al. 2007; Wallace etal. 2004a; Wallace and Stein 2007). However, these neurons were strikingly different from their normally reared counterparts, in that their ability to integrate crossmodal cues was severely altered by the dark-rearing. Intriguingly, substantial differences were noted in the effects of dark-rearing on SC versus cortical multisensory processes. Whereas in the visually deprived group the vast majority of multisensory neurons in the SC showed no significant changes in response upon crossmodal pairings (Wallace et al. 2004a), in AES the effect in many neurons was a transition from response enhancements to response depressions (Carriere et al. 2007). Here, pairings that typically resulted in significant response gains (i.e. enhancements, which could be additive or superadditive) in normally-reared animals resulted in significant response depressions. Such an outcome suggests that dark-rearing may alter the local circuit relations in the cortex such that inhibition is now favoured over excitation.

In addition to eliminating sensory experience in one modality, more recent experiments have examined the impact of altering the statistical relationships between multisensory stimuli early in development and then testing the consequent impact on these same circuits. As alluded to earlier, in ‘normal’ environments spatial and temporal proximity are powerful cues as to the relatedness of crossmodal cues. What happens if these cues are now yoked in ways that violate the normal physical world? To do this, cats were raised in environments in which the spatial relationship between visual and auditory stimuli was systematically altered. Here, the presentation of a visual stimulus was invariably linked to the presentation of an auditory cue from a different (but fixed) spatial location, violating the ‘typical’ circumstance in which these cues would normally be spatially congruent (and which likely serves as the substrate for the ‘spatial principle’ described earlier). After raising cats in such an environment, neurophysiological recordings from adults revealed a marked reorganization in the architecture and processing features of visual-auditory multisensory neurons (Wallace and Stein 2007). First, these neurons were found to have spatial receptive fields that had shifted in order to reflect the altered physical world. Thus, if the rearing environment was such that the auditory cues were always displaced by 30° relative to the visual cues, the receptive fields were found to be misaligned by a comparable amount. These findings closely parallel prior studies conducted in birds (i.e. owls—see Knudsen and Brainard 1991) and mammals (i.e. ferrets—see King et al. 1988), which demonstrated similar shifts in spatial representations with developmental perturbations. However, in the current work, we have extended these findings to show that this reordered receptive field architecture now forms the basis for the integrative capabilities of these neurons, such that stimuli separated by 30° were those that gave rise to the maximal multisensory interactions (Fig. 14.3).

Recently, preliminary studies have extended these findings into the temporal domain, and have shown that raising animals in a world in which visual and auditory stimuli are always presented in a spatially aligned but temporally disparate manner (i.e. a visual stimulus comes on and is followed by an auditory stimulus 100 ms later), results in a shift in the temporal-tuning functions of these neurons such that they ‘prefer’ the time lag experienced during postnatal life. Although still in their early stages, these experiments also suggest that there is a limit to the degree of temporal disparity that can be tolerated and still result in a neuron with significant interactive capabilities. When the visual and auditory stimuli were separated not by 100 ms, but by 250 ms, the ability of the neuron to support additive/superadditive interactions was abolished. This finding has important mechanistic implications, in that it suggests that there is a biophysical constraint on the integrative process, and narrows the list of likely cellular and molecular processes that govern the way in which multisensory inputs are synthesized.

Taken as a whole, these findings suggest a powerful role for sensory experience in shaping the final state of the multisensory processing circuits. In addition, these studies argue that sensory experience by itself is sufficient to engender substantial change in these developing circuits, a finding in keeping with the large body of work that has documented developmental plasticity in unisensory systems and in which alterations in the sensory statistics are sufficient to induce substantial change (for reviews see Katz and Crowley 2002; Hensch 2004, 2005). Furthermore, the inability of these same sensory manipulations to drive change in adult systems reinforces the concept of a sensitive period for multisensory plasticity. Waiting to be addressed is whether plasticity can be restored if these same statistical manipulations are paired with reinforcement, as has been shown for the individual sensory systems (Ahissar et al. 1992; Blake etal. 2006; Kilgard and Merzenich 1998).

The spatial constraints of multisensory integration appear dependant on the experiences received during development

Fig. 14.3 The spatial constraints of multisensory integration appear dependant on the experiences received during development. The figure shows data from two neurons, one from a control animal (A) and one from a spatial disparity reared animal (B). Top: receptive fields (visual, dark grey shading; auditory, light grey shading) of these neurons, along with the locations of the stimuli used to assess multisensory integration. Middle: responses of these neurons to visual, auditory and combined visual- auditory (i.e. multisensory) stimulation. Peristimulus time histograms depict the summed neural responses for a total of 15 trials for each condition with the ramps and square waves at the top showing the timing of the visual and auditory stimulus, respectively. Summary bar graphs at the bottom show the mean responses for each condition, along with the magnitude of the multisensory enhancement (furthest right bar in each graph) and predicted sum of the visual and auditory responses (dashed line). (Reproduced from Mark T. Wallace and Barry E. Stein, Early Experience Determines How the Senses Will Interact, Journal of Neurophysiology, 97 (1), pp. 921-926 © 2007 The American Physiological Society with permission.)

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