Multisensory enhancement of overt behavior requires multisensory experience

Smyre, Scott A.; Wang, Zhengyang; Stein, Barry E.; Rowland, Benjamin A.

doi:10.1111/ejn.15315

Cited by 14 publications

(14 citation statements)

References 64 publications

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“…These results are seemingly at odds with studies in dark reared cats in which no multisensory enhancement was found in multisensory neurons of the superior colliculus ( Wallace et al., 2004 ; Yu et al., 2019 ). Recently, however, multisensory gains in superior colliculus neurons have been observed when the animals were tested in light rather than in the dark ( Smyre et al., 2021 ). We conducted our experiment in a lit room and, moreover, unlike the previously tested dark-reared cats, the CC individuals of the present study had extensive experience with audio-visual stimuli in natural environments after cataract-removal surgery, many for several years.…”

Section: Discussionmentioning

confidence: 99%

“…Sensory experiences made during sensitive periods of development have a strong and lasting impact on how information from the different sensory systems is combined ( Putzar et al., 2007 ; Schorr et al., 2005 ; Smyre et al., 2021 ; Sourav et al., 2019 ; Wallace and Stein, 2007 ). For example, neuroanatomical and neurophysiological studies in owls have revealed distinct neural mechanisms for crossmodal recalibration depending on the age of the animals: Although crossmodal recalibration in juvenile owls was mediated by anatomical changes ( DeBello et al., 2001 ; Feldman and Knudsen, 1997 ), it was associated with top-down guided physiological changes in adult animals ( Hyde and Knudsen, 2002 ; Knudsen, 1998 ).…”

Section: Introductionmentioning

confidence: 99%

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Audiovisual spatial recalibration but not integration is shaped by early sensory experience

Bruns

Guerreiro

et al. 2022

iScience

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Audiovisual spatial recalibration but not integration is shaped by early sensory experience

Bruns

Guerreiro

et al. 2022

iScience

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“…Thus, lower ALFF in parietal cortex in the CC compared with the SC group might indicate a lower visual influence on multisensory (spatial) processing. Recently, Smyre et al 101 reported an impaired multisensory detection and localization in dark reared cats. In fact, two behavioural studies have found a reduced visual impact on tactile spatial performance in congenital cataract-reversal individuals with a history of longer lasting visual deprivation.…”

Section: Discussionmentioning

confidence: 99%

Typical resting-state activity of the brain requires visual input during an early sensitive period

Rączy

Hölig

Guerreiro

et al. 2022

Brain Communications

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Sensory deprivation, following a total loss of one sensory modality e.g. vision, has been demonstrated to result in compensatory plasticity. It is yet not known to which extent neural changes, e.g. higher resting state activity in visual areas (cross-modal plasticity) as a consequence of blindness, reverse, when sight is restored. Here, we used functional MRI to acquire blood oxygen level dependent (BOLD) resting state activity during an eyes open (EO) and an eyes closed (EC) state in congenital cataract-reversal individuals, developmental cataract-reversal individuals, congenitally permanently blind individuals and sighted controls. The amplitude of low frequency fluctuations (ALFF) of the BOLD signal - a neural marker of spontaneous brain activity during rest - was analyzed. In accord with previous reports, in normally sighted controls we observed an increase in ALFF during rest with the EO compared to rest with EC in visual association areas and in parietal cortex but a decrease in auditory and sensorimotor regions. In congenital cataract-reversal individuals, we found an increase of the amplitude of slow BOLD fluctuations in visual cortex during rest with EO compared to rest with EC too but this increase was larger in amplitude than in normally sighted controls. In contrast, congenital cataract-reversal individuals lagged a similar increase in parietal regions and did not show the typical decrease of ALFF in auditory cortex. Congenitally blind individuals displayed an overall higher amplitude in slow BOLD fluctuations in visual cortex compared to sighted individuals and compared to congenital cataract-reversal individuals in the EC condition. Higher ALFF in visual cortex of congenital cataract-reversal individuals than in normally sighted controls during EO might indicate an altered excitatory-inhibitory balance of visual neural circuits. By contrast, the lower parietal increase and the missing downregulation in auditory regions suggest a reduced influence of the visual system on multisensory and the other sensory systems after restoring sight in congenitally blind individuals. These results demonstrate a crucial dependence of visual and multisensory neural system functioning on visual experience during a sensitive phase in human brain development.

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“…Multisensory response enhancement (ME SF ) was calculated as the percent difference between the mean multisensory and most effective unisensory response calculated on a trial-by-trial basis via bootstrap, a metric referred to as “statistical facilitation” (SF) ( Miller, 1982 ; Otto et al, 2013 ; Nava et al, 2014 ; Wang et al, 2020 ; Smyre et al, 2021 ; Bean et al, 2022 ).…”

Section: Methodsmentioning

confidence: 99%

Predictability alters multisensory responses by modulating unisensory inputs

et al. 2023

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The multisensory (deep) layers of the superior colliculus (SC) play an important role in detecting, localizing, and guiding orientation responses to salient events in the environment. Essential to this role is the ability of SC neurons to enhance their responses to events detected by more than one sensory modality and to become desensitized (‘attenuated’ or ‘habituated’) or sensitized (‘potentiated’) to events that are predictable via modulatory dynamics. To identify the nature of these modulatory dynamics, we examined how the repetition of different sensory stimuli affected the unisensory and multisensory responses of neurons in the cat SC. Neurons were presented with 2HZ stimulus trains of three identical visual, auditory, or combined visual–auditory stimuli, followed by a fourth stimulus that was either the same or different (‘switch’). Modulatory dynamics proved to be sensory-specific: they did not transfer when the stimulus switched to another modality. However, they did transfer when switching from the visual–auditory stimulus train to either of its modality-specific component stimuli and vice versa. These observations suggest that predictions, in the form of modulatory dynamics induced by stimulus repetition, are independently sourced from and applied to the modality-specific inputs to the multisensory neuron. This falsifies several plausible mechanisms for these modulatory dynamics: they neither produce general changes in the neuron’s transform, nor are they dependent on the neuron’s output.

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Multisensory enhancement of overt behavior requires multisensory experience

Cited by 14 publications

References 64 publications

Audiovisual spatial recalibration but not integration is shaped by early sensory experience

Audiovisual spatial recalibration but not integration is shaped by early sensory experience

Typical resting-state activity of the brain requires visual input during an early sensitive period

Predictability alters multisensory responses by modulating unisensory inputs

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