Elsevier

Cortex

Volume 49, Issue 4, April 2013, Pages 1100-1109
Cortex

Research report
The influence of preterm birth on structural alterations of the vision-deprived brain

https://doi.org/10.1016/j.cortex.2012.03.013Get rights and content

Abstract

Differences in brain structures between blind and sighted individuals have not been widely investigated. Furthermore, existing studies have included individuals who were blinded by retinopathy of prematurity, a condition that is associated with premature birth. Recent pediatric research has reported structural differences in individuals who were born prematurely, suggesting that some of the structural abnormalities previously observed in blind individuals may be related to prematurity rather than being specific to blindness. In the present study, we used voxel-based morphometry to investigate gray and white matter differences between 24 blind and 16 sighted individuals. Of the blind individuals, six were born prematurely and 18 at term. Compared to those born at term, blind individuals born preterm showed differences in gray, but not white, matter volumes in various brain regions. When the preterm individuals were excluded from analysis, there were significant differences between blind and sighted individuals. Full-term blind individuals showed regional gray matter decreases in the cuneus, lingual gyrus, middle occipital gyrus, precuneus, inferior and superior parietal lobules, and the thalamus, and gray matter increases in the globus pallidus. They also showed regional white matter decreases in the cuneus, lingual gyrus, and the posterior cingulate. These differences were observed in blind individuals irrespective of blindness onset age, providing evidence for structural alterations in the mature brain. Our findings highlight the importance of considering the potential impact of premature birth on neurodevelopmental outcomes in studies of blind individuals.

Introduction

Neuroimaging studies of blind individuals have revealed the effects of visual deprivation on the organization of the human brain. Over the past decade, there has been growing evidence that implicates the occipital cortex in the processing of non-visual stimuli by blind individuals. This cross-modal plasticity has been observed in a variety of studies using tactile (Burton et al., 2004, 2002; Gizewski et al., 2003; Sadato et al., 1998, 1996; Thompson et al., 2008), verbal linguistic (Amedi et al., 2003; Burton et al., 2003), and auditory stimuli (Stevens and Weaver, 2005; Voss et al., 2006; Weeks et al., 2000). The functional relevance of the occipital cortex in non-visual processing has been demonstrated by transcranial magnetic stimulation (Pascual-Leone and Torres, 1993) and lesion (Hamilton et al., 2000) studies. In addition, experiments with blindfolded sighted individuals have demonstrated cross-modal activation during non-visual task performance (e.g., Pascual-Leone and Hamilton, 2001), suggesting that plastic changes can occur throughout life.

In contrast to the vast literature on functional reorganization, only a handful of studies have examined structural changes in blind individuals. In sighted individuals, several studies have shown that structural changes are associated with environmental demands in terms of increased volumes of specific brain structures (e.g., the hippocampus in taxi drivers, Maguire et al., 2000; the mid-temporal area in practiced jugglers, Draganski et al., 2004; the posterior parietal region and hippocampus in students preparing for exams, Draganski et al., 2006). In blind individuals, studies investigating structural brain changes have shown that their visual areas are smaller, a change that may be detected with radiological inspection (Breitenseher et al., 1998). More sophisticated analysis such as voxel-based morphometry (VBM) has revealed a reduction in gray matter volume in the primary and secondary visual areas, as well as atrophy of the optic chiasm and optic radiation (Noppeney et al., 2005; Pan et al., 2007). In addition to these areas, Ptito et al. (2008) observed gray matter decreases in the precuneus and middle temporal regions. As a complement to the investigation of gray matter, diffusion tensor imaging (DTI) showed lower white matter densities in the visual cortices, and atrophy of the geniculo-calcarine tracts in five congenitally blind individuals (Shimony et al., 2006). In another DTI study (Schoth et al., 2006), no such differences were observed between sighted controls and six blind individuals. More recent structural imaging studies have reported decreased connectivity in the inferior frontal and occipital lobes (Shu et al., 2009), and thicker cortical surface of visual areas (Jiang et al., 2009) in blind compared to sighted individuals.

In non-visual brain areas, structural changes have not been consistently observed. For example, Shimony et al. (2006) reported white matter increases in the primary somatosensory and motor areas. In contrast, Ptito et al., (2008) reported white matter decreases in the splenium of the corpus callosum and the inferior longitudinal fasciculus, and Pan et al. (2007) observed white matter decreases in the temporal lobe. A possible reason for the mixed findings could be the inclusion of blind individuals born prematurely. One of the most common causes of congenital or early blindness is retinopathy of prematurity (ROP), which results from high levels of supplemental oxygen administered following premature birth (Smith, 2003). Recent studies on preterm sighted infants have revealed significantly smaller volumes of gray matter tissues compared to full-term infants (e.g., Boardman et al., 2006; Cheong et al., 2008; Thompson et al., 2008), a change which persists to adolescence (Nosarti et al., 2008) and adulthood (Parker et al., 2008). Some of the areas affected include the putamen, insula, cuneus, fusiform gyrus, thalamus, caudate nucleus, and lentiform nucleus. Given the effects of premature birth in sighted individuals, it is likely that premature birth would also lead to structural changes in blind individuals.

Most existing neuroimaging studies on blindness-induced brain reorganization have included individuals with ROP. It is therefore possible that prematurity, rather than blindness, contributes to some of the structural changes previously reported. For example, three of five participants in Shimony et al. (2006) and four of 11 participants in Ptito et al., (2008) suffered from ROP. In Noppeney et al. (2005), five of 11 participants were congenitally blind, and ROP was listed as one of the causes of blindness in their participants.

The present study used VBM to examine region-specific changes in gray and white matter as a result of complete blindness. In addition, because many studies have shown that premature birth can lead to considerable changes in brain structures, at least in sighted individuals, we were motivated to examine the effect of prematurity in blind individuals.

Section snippets

Participants

24 blind volunteers (mean age 42 years, age range 21–63) and 16 sighted controls (mean age 37 years, age range 22–53) participated in this study. All were right-handed. In all blind participants, blindness was caused by peripheral defects. At the time of testing, blind individuals had no pattern vision, and minimal (or no) sensitivity to light. Furthermore, they had no significant hearing loss, as assessed by an audiogram. All participants were reported to have no neurological or psychiatric

Results

The total (i.e., global) gray and white matter volumes were compared between the various groups of blind and sighted individuals. Relative to the sighted controls, the blind participants showed significantly lower total white matter volumes, t(38) = −3.202, p = .003, but no differences in total gray matter volumes, t(38) = −1.744, p = .09. To examine whether preterm birth affected total brain volumes, blind individuals born preterm were compared with those born at term. All preterm individuals

Discussion

The present study examined structural differences in the brains of blind and sighted individuals. We included a relatively large number of blind individuals in our analyses, and considered the effects of premature birth on brain reorganization. First, we found that the total volumes of white matter tissue were smaller in the blind group, but there were no significant differences between blind individuals born preterm and those born at term. Second, when we compared all blind individuals with

Conclusion

Our study demonstrated gray and white matter differences between blind and sighted individuals. Those who became blind later in life also showed variation in brain tissue volumes compared to sighted controls, suggesting that structural changes may also be possible in adults. Importantly, our findings showed that blind individuals born prematurely had significantly different brain tissue volumes compared to those born full-term. Given that a common cause of complete blindness is ROP, future

Acknowledgments

A.G.W. was supported by a National Health and Medical Research Council Clinical Research Training Fellowship (251755). We would like to thank Robert Lindenberg for his comments.

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