Missing sights: consequences for visual cognitive development

doi:10.1016/j.tics.2005.01.006

Trends in Cognitive Sciences

Volume 9, Issue 3, March 2005, Pages 144-151

https://doi.org/10.1016/j.tics.2005.01.006 Get rights and content

The effects of early-onset blindness on the development of the visual system have been explained traditionally by the stabilization of transient connections through Hebbian competition. Although many of the findings from congenital cataract and congenital blindness are consistent with that view, there is inconsistent evidence from studies of visual cognition in children treated for visual deprivation from cataract, case reports of recovery of vision in adults, and studies of visual reorganization after late-onset blindness. Collectively, the data from congenital cataract and congenital blindness indicate that early visual experience sets up the infrastructure for later learning involving both the dorsal (‘where’) and ventral (‘what’) streams. Nevertheless, there is surprising residual plasticity in adulthood that can be revealed if vision is lost either temporarily or permanently. This has important implications for understanding the role of early visual experience in shaping visual cognitive development.

Introduction

Human visual acuity improves fivefold in the first 6 months after birth and continues to improve over the next 6 years [1]. The final acuity is abnormal if early visual input was blocked by cataracts, with a larger impairment in the affected eye(s) if the deprivation was monocular rather than binocular and if the deprivation occurred earlier in life [2]. As with animal studies 3, 4, these results suggest that early visual deprivation during a sensitive period causes permanent damage to the primary visual cortex and presumably the higher visual areas to which it projects, with a worse outcome if there was also uneven competition for cortical synapses between a non-deprived eye and a treated eye. Recent studies have indicated that when visual input is missing permanently because of congenital blindness, the visual cortex becomes specialized for the processing of touch and sound instead of vision. These findings can be explained by a shaping of otherwise transient connections through a process of Hebbian competition in which stronger input signals win out and unused connections are pruned permanently. However, the generality of these patterns and their interpretation by Hebbian competition has been called into question (i) by recent studies of children treated for cataract that followed patients longitudinally and that included measures of higher visual functions; (ii) by case reports of surprising recovery of vision under some circumstances in adulthood; and (iii) by studies of visual re-organization after late-onset blindness. This review considers the implications of these findings for understanding the role of early visual input in shaping normal visual cognitive development.

Section snippets

Cataract-reversal patients

Children born with bilateral or unilateral cataracts provide a natural experiment to assess the effects on human development of early deprivation and of unequal competition between the eyes for cortical connections. A cataract is an opacity in the lens of the eye which, if large and dense, allows only diffuse light to reach the retina. Pattern deprivation continues until the defective natural lens of the eye is removed surgically and the eye is fitted with a compensatory optical correction

Congenital blindness

Another natural experiment for studying visual plasticity is provided by children born with non-reversible blindness, such that the visual cortex never receives input from external visual stimuli. Recent imaging studies of adults who were blind from an early age indicate that the visual cortex can be recruited for processing tactile and auditory input [20]. For example, tactile input from reading Braille or discriminating between complex tactile patterns activates the visual cortex almost as

Neural mechanisms of visual cortical reorganization: Hebbian competition?

The traditional explanation of the effects of congenital blindness is the stabilization of transient connections among sensory cortical areas that are present in early infancy [20]. There is anatomical evidence for such exuberant connections in humans [32], as in animals [33], and some indication that they are functional during infancy: spoken language elicits a large event-related potential (ERP) over the temporal cortex in infants, as it does in adults, but in infants it also elicits a large

Beyond Hebbian competition

The pruning effected by Hebbian competition is believed to leave the visual nervous system more-or-less permanently rewired and to ramify through to higher cortical areas that receive their main input from primary sensory cortical areas. However, recent studies indicate that some exuberant connections are inhibited rather than pruned and that, for some visual functions, there is visual plasticity even in adolescence and adulthood – well beyond the period of synaptic pruning. Furthermore, the

Early experience can be important to preserve the infrastructure for later learning, without any learning taking place at the earlier time

Children treated for bilateral congenital cataracts as early as 2–3 months of age fail to develop normal holistic face processing and normal sensitivity to the spacing of facial features (15, 19; see Table 1). Yet the first signs of these capabilities do not appear in the visually normal infant until later during infancy [55] and sensitivity to the spacing of facial features is not adult-like until after 14 yrs of age [56]. There is a similar pattern for visual acuity: by their first birthday,

Conclusions

Studies of adults with a history of early visual deprivation from cataract or permanent blindness indicate that early sensory input plays an important role in setting up the infrastructure for later tuning of the visual cortex. When visual input is delayed until cataracts are removed, there is only partial recovery of visual capabilities. When visual input is missing permanently because of blindness, the visual cortex becomes specialized for touch and hearing. To a large extent, these changes

Acknowledgements

Supported by grants from the National Science and Engineering Council of Canada and the Canadian Institutes of Health Research to Daphne Maurer.

References (69)

D. Maurer et al.
Visual acuity: the role of visual input in inducing postnatal change
Clin. Neurosci. Res.
(2001)
D. Ellemberg
Spatial and temporal vision in patients treated for bilateral congenital cataracts
Vision Res.
(1999)
D. Ellemberg
The development of spatial and temporal vision during childhood
Vision Res.
(1999)
C. Mondloch
Developmental changes in face processing skills
J. Exp. Child Psychol.
(2003)
T.L. Lewis
Sensitivity to global form in glass patterns after early visual deprivation in humans
Vision Res.
(2002)
D. Ellemberg
Better perception of global motion after monocular than after binocular deprivation
Vision Res.
(2002)
B.G. Jeffrey
Altered global shape discrimination in deprivation amblyopia
Vision Res.
(2004)
H. Théoret
Behavioral and neuroplastic changes in the blind: evidence for functionally relevant cross-modal interactions
J. Physiol. (Paris)
(2004)
E. Gizewski
Cross-modal plasticity for sensory and motor activation patterns in blind subjects
Neuroimage
(2003)
N. Sadato
Critical period for cross-modal plasticity in blind humans: A functional MRI study
Neuroimage
(2002)

T. Kujala

Visual cortex activation in blind humans during sound discrimination

Neurosci. Lett.

(1995)

B. Röder

Event-related potentials during auditory language processing in congenitally blind and sighted people

Neuropsychologia

(2000)

J. Wattam-Bell

Coherence thresholds for discrimination of motion direction in infants

Vision Res.

(1994)

D. Ellemberg

Influence of monocular deprivation during infancy on the later development of spatial and temporal vision

Vision Res.

(2000)

Lewis, T.L. and Maurer, D. Multiple sensitive periods in human visual development: Evidence from visually deprived...

D.E. Mitchell et al.

The present and potential impact of research in animal models for clinical treatment of deprivation amblyopia

Clin. Exp. Optom.

(2002)

N.W. Daw

Critical periods in the visual system

Maurer, D. et al. (1989) The effects of deprivation on human visual development: Studies of children treated for...

S. Geldart

The effects of early visual deprivation on the development of face processing

Dev. Sci.

(2002)

C.J. Mondloch

Configural face processing develops more slowly than featural face processing

Perception

(2002)

D. Maurer

Rapid improvement in the acuity of infants after visual input

Science

(1999)

Ellemberg, D. et al. (2001) The role of visual input in setting up spatial filters in the human visual system....

G. Magnusson

Changes in visual acuity from 4 to 12 years of age in children operated for bilateral congenital cataracts

Br. J. Ophthalmol.

(2002)

A. Lundvall et al.

Outcome after treatment for congenital bilateral cataract

Acta Ophthalmol. Scand.

(2002)

Le Grand, R. et al. (2001) Early visual experience and face processing. Nature 410, 890; Correction. 412,...

R. Le Grand

Impairment in holistic face processing following early visual deprivation

Psychol. Sci.

(2004)

H. Burton

Adaptive changes in early and late blind: a fMRI study of Braille reading

J. Neurophysiol.

(2002)

L. Cohen

Period of susceptibility for cross-modal plasticity in the blind

Ann. Neurol.

(1999)

B. Röder

Speech processing activates visual cortex in congenitally blind humans

Eur. J. Neurosci.

(2002)

D. Bavelier et al.

Cross-modal plasticity: Where and how?

Nat. Rev. Neurosci.

(2002)

A. Amedi

Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind

Nat. Neurosci.

(2003)

H. Burton

Dissociating cortical regions activated by semantic and phonological tasks: a fMRI study in blind and sighted people

J. Neurophysiol.

(2003)

R. Yaka

Auditory activation of cortical visual areas in cats after early visual deprivation

Eur. J. Neurosci.

(1999)

P. Huttenlocher

Synaptogenesis in human cerebral cortex

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The timing of the developmental emergence of holistic face processing and its sensitivity to experience in early childhood are somewhat controversial topics. To investigate holistic face perception in early childhood, we used an online testing platform and administered a two-alternative forced-choice task to 4-, 5-, and 6-year-old children. The children saw pairs of composite faces and needed to decide whether the faces were the same or different. To determine whether experience with masked faces may have negatively affected holistic processing, we also administered a parental questionnaire to assess the children’s exposure to masked faces during the COVID-19 pandemic. We found that all three age groups performed holistic face processing when the faces were upright (Experiment 1) but not when the faces were inverted (Experiment 2), that response accuracy increased with age, and that response accuracy was not related to degree of exposure to masked faces. These results indicate that holistic face processing is relatively robust in early childhood and that short-term exposure to partially visible faces does not negatively affect young children’s holistic face perception.
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Citation Excerpt :
Attention to and learning about these visual stimuli is important for development. Infants born with dense central cataracts suffer vision deficits throughout their lives, even when vision is restored early in infancy (Maurer, 2017; Maurer, Lewis, & Mondloch, 2005). Moreover, this limited visual ability early in infancy is important for constraining the input, which may be critical for development (Mareschal et al., 2007).
Visual attention develops rapidly and significantly during the first postnatal years. At birth, infants have poor visual acuity, poor head and neck control, and as a result have little autonomy over where and how long they look. Across the first year, the neural systems that support alerting, orienting, and endogenous attention develop, allowing infants to more effectively focus their attention on information in the environment important for processing. However, visual attention is a system that develops in the context of the whole child, and fully understanding this development requires understanding how attentional systems interact and how these systems interact with other systems across wide domains. By adopting a cascades framework we can better position the development of visual attention in the context of the whole developing child. Specifically, development builds, with previous achievements setting the stage for current development, and current development having cascading consequences on future development. In addition, development reflects changes in multiple domains, and those domains influence each other across development. Finally, development reflects and produces changes in the input that the visual system receives; understanding the changing input is key to fully understand the development of visual attention. The development of visual attention is described in this context.
Steady state evoked potentials indicate changes in nonlinear neural mechanisms of vision in sight recovery individuals
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Humans with a transient phase of congenital pattern vision deprivation have been observed to feature prevailing deficits, particularly in higher order visual functions. However, the neural correlates of these prevalent visual impairments remain unclear. To probe different visual processing stages, we measured steady state visual evoked potentials (SSVEPs) generated by luminance flicker stimuli at 6.1 Hz, with superimposed horizontal periodic motion at 2.1 Hz or 2.4 Hz. SSVEP responses at the fundamental and second harmonic of luminance flicker frequency, and at their intermodulation frequencies with motion information, were analyzed. Three groups were tested: (1) 15 individuals who had suffered a lack of pattern vision from birth due to the presence of bilateral total congenital cataracts (CC group), which were surgically removed between 4 months and 22 years of age, (2) 13 individuals with reversed developmental i.e., later developing cataracts (DC group), and (3) normally sighted control participants (SC group; n = 13) matched in age and sex to the CC individuals. SSVEPs at the second harmonic frequency (i.e., 12.2 Hz) and at the intermodulation frequencies (8.2 Hz, and 8.5 Hz) were attenuated in the CC group. In contrast, fundamental frequency responses (i.e., at 6.1 Hz) were not significantly altered in the CC group compared to the control groups (SC and DC groups). Based on previous evidence on the role of striate vs. extrastriate generators of fundamental vs. second harmonics of SSVEPs, these results provide evidence for a stronger experience dependence of extrastriate than striate cortical processing, and furthermore, suggest a sensitive period for the development of putative nonlinear neural mechanisms hypothesized to mediate visual feature binding.
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The ability to encode space is a crucial aspect of interacting with the external world. Therefore, this ability appears to be fundamental for the correct development of the capacity to integrate different spatial reference frames. The spatial reference frame seems to be present in all the sensory modalities. However, it has been demonstrated that different sensory modalities follow various developmental courses. Nevertheless, to date these courses have been investigated only in people with sensory impairments, where there is a possible bias due to compensatory strategies and it is complicated to assess the exact age when these skills emerge. For these reasons, we investigated the development of the allocentric frame in the auditory domain in a group of typically developing children aged 6–10 years. To do so, we used an auditory Simon task, a paradigm that involves implicit spatial processing, and we asked children to perform the task in both the uncrossed and crossed hands postures. We demonstrated that the crossed hands posture affected the performance only in younger children (6–7 years), whereas at 10 years of age children performed as adults and were not affected by such posture. Moreover, we found that this task’s performance correlated with age and developmental differences in spatial abilities. Our results support the hypothesis that auditory spatial cognition’s developmental course is similar to the visual modality development as reported in the literature.
Neuroplasticity of the visual cortex: in sickness and in health
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Brain plasticity refers to the ability of synaptic connections to adapt their function and structure in response to experience, including environmental changes, sensory deprivation and injuries. Plasticity is a distinctive, but not exclusive, property of the developing nervous system. This review introduces the concept of neuroplasticity and describes classic paradigms to illustrate cellular and molecular mechanisms underlying synapse modifiability. Then, we summarize a growing number of studies showing that the adult cerebral cortex retains a significant degree of plasticity highlighting how the identification of strategies to enhance the plastic potential of the adult brain could pave the way for the development of novel therapeutic approaches aimed at treating amblyopia and other neurodevelopmental disorders. Finally, we analyze how the visual system adjusts to neurodegenerative conditions leading to blindness and we discuss the crucial role of spared plasticity in the visual system for sight recovery.
Neuroplasticity in adult human visual cortex
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Between 1-5:100 people worldwide have never experienced normotypic vision due to a condition called amblyopia, and about 1:4000 suffer from inherited retinal dystrophies that progressively lead to blindness. While a wide range of technologies and therapies are being developed to restore vision, a fundamental question still remains unanswered: would the adult visual brain retain a sufficient plastic potential to learn how to ‘see’ after a prolonged period of abnormal visual experience? In this review we summarize studies showing that the visual brain of sighted adults retains a type of developmental plasticity, called homeostatic plasticity, and this property has been recently exploited successfully for adult amblyopia recovery. Next, we discuss how the brain circuits reorganize when blindness occurs and when visual stimulation is partially restored by means of a ‘bionic eye’ in late blind adults with Retinitis Pigmentosa. The primary visual cortex in these patients slowly became activated by the artificial visual stimulation, indicating that sight restoration therapies can rely on a considerable degree of spared plasticity in adulthood.

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View full text

Trends in Cognitive Sciences

Missing sights: consequences for visual cognitive development

Introduction

Section snippets

Cataract-reversal patients

Congenital blindness

Neural mechanisms of visual cortical reorganization: Hebbian competition?

Beyond Hebbian competition

Early experience can be important to preserve the infrastructure for later learning, without any learning taking place at the earlier time

Conclusions

Acknowledgements

Clin. Neurosci. Res.

Vision Res.

Vision Res.

J. Exp. Child Psychol.

Vision Res.

Vision Res.

Vision Res.

J. Physiol. (Paris)

Neuroimage

Neuroimage

Neurosci. Lett.

Neuropsychologia

Vision Res.

Vision Res.

The present and potential impact of research in animal models for clinical treatment of deprivation amblyopia

Clin. Exp. Optom.

Critical periods in the visual system

The effects of early visual deprivation on the development of face processing

Dev. Sci.

Configural face processing develops more slowly than featural face processing

Perception

Rapid improvement in the acuity of infants after visual input

Science

Changes in visual acuity from 4 to 12 years of age in children operated for bilateral congenital cataracts

Br. J. Ophthalmol.

Outcome after treatment for congenital bilateral cataract

Acta Ophthalmol. Scand.

Impairment in holistic face processing following early visual deprivation

Psychol. Sci.

Adaptive changes in early and late blind: a fMRI study of Braille reading

J. Neurophysiol.

Period of susceptibility for cross-modal plasticity in the blind

Ann. Neurol.

Speech processing activates visual cortex in congenitally blind humans

Eur. J. Neurosci.

Cross-modal plasticity: Where and how?

Nat. Rev. Neurosci.

Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind

Nat. Neurosci.

Dissociating cortical regions activated by semantic and phonological tasks: a fMRI study in blind and sighted people

J. Neurophysiol.

Auditory activation of cortical visual areas in cats after early visual deprivation

Eur. J. Neurosci.

Synaptogenesis in human cerebral cortex