Review
The role of visual experience for the neural basis of spatial cognition

https://doi.org/10.1016/j.neubiorev.2012.01.008Get rights and content

Abstract

Blindness often results in the adaptive neural reorganization of the remaining modalities, producing sharper auditory and haptic behavioral performance. Yet, non-visual modalities might not be able to fully compensate for the lack of visual experience as in the case of congenital blindness. For example, developmental visual experience seems to be necessary for the maturation of multisensory neurons for spatial tasks. Additionally, the ability of vision to convey information in parallel might be taken into account as the main attribute that cannot be fully compensated by the spared modalities. Therefore, the lack of visual experience might impair all spatial tasks that require the integration of inputs from different modalities, such as having to represent a set of objects on the basis of the spatial relationships among the objects, rather than the spatial relationship that each object has with oneself. Here we integrate behavioral and neural evidence to conclude that visual experience is necessary for the neural development of normal spatial cognition.

Highlights

► Blindness produces adaptive neural reorganization in non-visual modalities. ► Congenital blindness might negatively affect allocentric spatial representation. ► Developmental visual experience might be necessary for multisensory integration for spatial cognition. ► The brain areas involved in spatial processing are multisensory integration centers. ► Visual experience might be necessary to fully develop the brain areas necessary for normal multisensory integration and spatial cognition.

Introduction

The study of blind individuals affords a unique opportunity to investigate the role of vision for a wide range of cognitive and perceptual processes and on brain development. More importantly, by distinguishing between congenital and late blind, we can assess the developmental role of the visual experience for a variety of cognitive phenomena. In this review we will initially discover that the lack of vision produces adaptive reorganization in the spared modalities. Then we will narrow down our attention to focus on spatial tasks. In particular we will review the way visual experience affects other modalities, its role for multisensory integration, and how visual experience impacts the brain areas involved in spatial processing. We suggest that visual experience might be crucial to develop the multisensory integration necessary for normal spatial cognition.

Traditionally it has been suggested that the lack of vision sharpens the remaining modalities (James, 1890) and a vast number of empirical studies reported that blind individuals showed unimpaired or even superior tactile and auditory discrimination and localization, verbal processing, memory span and long term memory (Alary et al., 2008, Amedi et al., 2003, D’Angiulli and Waraich, 2002, D’Angiulli et al., 1998, Hamilton et al., 2004, Heller, 1989, Hull and Mason, 1995, Lessard et al., 1998, Norman and Bartholomew, 2011, Postma et al., 2007, Raz et al., 2007, Röder et al., 1999, Smith et al., 2005, Voss et al., 2004, Goldreich and Kanics, 2003, Goldreich and Kanics, 2006).

Moreover, neuroimaging studies found that the visual areas of blind individuals are active during the processing of auditory, haptic and olfactory stimuli (Amedi et al., 2003, Burton et al., 2002, Kupers et al., 2011, Noppeney et al., 2003, Röder et al., 2002, Sadato et al., 1996, Thaler et al., 2011, Van Boven et al., 2000), suggesting that the aforementioned superior abilities of blind individuals are supported by the recruitment of the visual cortex by the remaining modalities. Additionally, studies on blind individuals investigating the effect of virtual and real lesions of the occipital lobe confirmed that the activation of visual areas during cognitive tasks was functionally relevant (Amedi et al., 2004, Cohen et al., 1997, Gougoux et al., 2005, Hamilton et al., 2000, Kupers et al., 2007, Merabet et al., 2009). For example, an fMRI study by Sadato et al. (1996) reported V1 activity during Braille reading in blind participants. The causal nature of this activity was evidenced by Hamilton et al. (2000), who reported the case of a blind person who developed Braille alexia following a bilateral occipital stroke.

The recruitment of visual areas has been found to be more common for congenitally blind individuals (Büchel et al., 1998, Stevens and Weaver, 2009, Veraart et al., 1990) and involves both gray and white brain matter (Shimony et al., 2006, Noppeney et al., 2005, Ptito et al., 2008), suggesting that early onset of blindness produces extensive brain reorganization. Studies involving the use of sensory substitution devices (SSD), where the input for a missing modality is conveyed by another sense (see Bach-y-Rita, 1972, Proulx, 2010), showed that congenitally blind individuals displayed increased activity in occipital ‘visual’ cortical areas during the use of a tactile-to-visual SSD that displays images on the tongue, while such activation was not found in sighted participants (Ptito et al., 2005). In addition, TMS stimulation of the visual cortex produced somatotopic sensations (i.e. qualia, see Proulx and Stoerig, 2006) on the tongue (i.e. the novel source of input to the visual cortex) of blind but not of sighted individuals (Kupers et al., 2006). This demonstrated the functional recruitment of visual cortex in the perception of a purely tactile input via the tongue that nonetheless gave rise to visual experience with sensory substitution.

Thus the above studies suggest that, following the recruitment of the otherwise unused visual cortex (perhaps due to practice, see Wong et al., 2011), non-visual sensory modalities can successfully compensate for the lack of vision and the blind can perform at the same level and even better than sighted individuals in a variety of non-visual tasks.

Section snippets

The impact of blindness on spatial tasks

Nevertheless, discordant results have been reported by studies investigating spatial cognition in blind individuals by using tasks such as memory for arrays of objects lying within the manipulatory space (arm's length), environmental knowledge, and navigation. In fact, some researchers found results suggesting that blindness, especially if congenital, prejudices the complete development of spatial cognition by rendering their spatial performance poorer than sighted and late blind participants (

The special nature of vision for spatial tasks

The difficulty of dealing with the allocentric reference frame and complex spatial representation might owe its explanation to the sequential (or serial, see Henriques and Soechting, 2005) nature of non-visual modalities, in particular haptics. In a classic study, Loomis et al. (1991) tested sighted participants by reducing their visual field (i.e. replicating the effect of looking through a tube) and found that, by forcing a serial acquisition of visual information, the recognition of objects

Is visual experience necessary for the full development of multisensory integration?

The studies investigating the role of vision in multisensory integration might help to shed light on the peculiar role of visual experience in complex, multidimensional spatial tasks. Multisensory integration reaches its maturation during the early years after birth (Gori et al., 2008, Lewkowicz and Lickliter, 1994). Postnatal experience is necessary for the full development of multisensory integration because multisensory neurons need to acquire the ability to respond to simultaneously

Multisensory integration for spatial cognition: impairment by early blindness

According to the ideas expressed in the previous section, the role of vision in multisensory integration was also found in tasks involving a spatial component and, more precisely, in studies investigating the role of visual experience in the integration of multisensory inputs within a common reference frame for perception and action planning. For example, Röder et al. (2004), involved participants with different levels of visual experience in a task where they judged the temporal order of

The neural basis of spatial cognition

The results described in the previous section suggest that visual experience promotes the remapping of multisensory inputs into a visually defined external reference frame. To this point, Sereno et al. (2001) reported the existence of retinotopic maps to integrate multisensory inputs in the human parietal lobe (see also Sereno and Huang, 2006). Thus, it might be the case that the lack of visual experience impacts the development of such topographic maps. Retinotopic maps are ideal for

The basis of spatial cognition in the blind brain

Studies on primates showed that the lack of visual experience affects the functionality of the neurons of the PPC (Hyvärinen et al., 1981) and that this effect persists when vision is regained (Carlson et al., 1987). Although Bonino et al. (2008) found that early blind participants activated the classical pattern of neural activity associated with spatial computation (including the PPC), studies trying to assess the role of the visual experience on human PPC and, more generally, on the dorsal

Neural plasticity in the metamodal brain

In our review we reported numerous empirical studies suggesting that developmental vision might be necessary for the full development of spatial cognition, possibly due to its ability of effortlessly conveying parallel information. Vision might also provide a basis for the topographic representation necessary for an allocentric reference frame and multisensory integration.

Nevertheless, this renders even more remarkable the ability of the brain to reorganize itself to overcome the lack of such a

Conclusion

Visual experience seems to be necessary for multisensory integration. In fact, several multisensory brain structures need early visual experience to develop the ability to integrate and represent multisensory information normally. In turn this produces a deficit in spatial tasks, especially if allocentric spatial representations or survey knowledge are required. This might have to do with the development of retinotopic maps in the cortical areas involved in spatial computation and

Acknowledgment

This work was supported by a Marie Curie Intra-European Fellowship (grant number: PIEF-GA-2010-274163).

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