Visual experience shapes functional connectivity between occipital and non-visual networks

Relative to sighted adults, visual cortices of adults born blind show enhanced responses during non-visual tasks, such as reading braille and localizing sounds as well as distinctive patterns of long-range functional connectivity with non-visual networks (Abboud and Cohen, 2019; Bedny et al., 2011; Burton et al., 2012; Burton et al., 2014; Butt et al., 2013; Collignon et al., 2011; Deen et al., 2015; Kanjlia et al., 2016; Kanjlia et al., 2021; Lane et al., 2015; Liu et al., 2007; Sadato et al., 1996; Striem-Amit et al., 2015; Watkins et al., 2012). Since almost all research thus far has been done with adults, a key outstanding question concerns the developmental origins of these experience-based differences.

One possibility is that at birth, infant visual cortices start out in the ‘prepared’ sighted adult state and blindness modifies this functional connectivity. Alternatively, infant visual cortices may start out functionally similar to those of blind adults, and lifetime visual experience shapes connectivity toward the sighted adult pattern. To distinguish between these possibilities, we compare the long-range function connectivity of visual cortices across blind adults, sighted adults, and a large cohort of 2-week-old infants (Developing Human Connectome Project, dHCP, n = 475). Using resting-state data provide a common measure of cortical function across these diverse populations.

To our knowledge, no prior studies have compared infants to multiple populations of adults with different sensory experiences. Previous studies comparing infants to sighted adults have largely reported similarity across groups (Barttfeld et al., 2018; Doria et al., 2010; Fransson et al., 2009; Gao et al., 2009; Liu et al., 2008; Zhang et al., 2019). However, these studies focused on whether large-scale functional networks are present in infancy, for example, stronger connectivity of regions within the visual network than between visual and auditory regions. Studies comparing blind and sighted adults find differences across groups in which non-visual networks are most strongly coupled with the visual system, that is, visual cortices of sighted adults show stronger coupling with non-visual sensory-motor networks (i.e., auditory, somatosensory/motor) than higher-cognitive systems; by contrast, in blind adults, visual cortex coupling is stronger with higher-cognitive prefrontal cortices (PFC) than with non-visual sensory-motor networks (Abboud and Cohen, 2019; Bedny et al., 2011; Burton et al., 2014; Deen et al., 2015; Kanjlia et al., 2021; Liu et al., 2007; Qin et al., 2013; Striem-Amit et al., 2015; Watkins et al., 2012; Yu et al., 2008). In the current study, we compare this experience-sensitive functional signature across infants, sighted, and blind adults.

We measured the connectivity profile of four occipital ‘visual’ areas that show cross-modal plasticity in blindness, that is, are active during non-visual tasks in blind people and show related changes in resting-state functional connectivity.

We focused on three functionally distinct secondary visual areas (located in lateral, dorsal, and parts of the ventral occipital cortex) and the primary visual cortex (V1). The three secondary visual areas have been found to respond to different non-visual tasks in blind people: language tasks, numerical reasoning tasks, and executive control tasks, respectively. Enhanced coupling with PFC is observed across all three occipital regions in blind adults. However, each region shows preferential coupling with a distinct subregion of PFC with analogous functional profiles, that is, language responsive occipital areas are more coupled with language responsive PFC (Kanjlia et al., 2016; Kanjlia et al., 2021; Lane et al., 2015). These observations suggest that resting-state and task-based functional profiles are related, although the functional and developmental nature of this relationship remains an open question.

The precise visual functions of the studied secondary visual regions in sighted people are not known. Anatomically, these regions in sighted people approximately correspond to the locations of motion-sensitive V5/MT+ and the lateral occipital complex (LO), as well as ventral portions of occipito-temporal cortex including V4v and dorsal portions including V3a. The occipital region of interest (ROI) also extends ventrally into the middle portion of the ventral temporal lobe and dorsally into the intraparietal sulcus and superior parietal lobule (Tootell et al., 1997; Van Essen et al., 2001).

We also examined connectivity of anatomically defined primary visual cortex (V1), which likewise shows altered task-based responses and functional connectivity in congenitally blind adults (Amedi et al., 2003; Bedny et al., 2011; Burton et al., 2014; Butt et al., 2013; Lane et al., 2015; Raz et al., 2005; Sadato et al., 1996; Striem-Amit et al., 2015; Yu et al., 2008). Since many previous studies have found that blindness alters the balance of connectivity between visual cortex and higher-order prefrontal as opposed to sensory-motor regions, this was our primary outcome measure (Abboud and Cohen, 2019; Bedny et al., 2011; Burton et al., 2014; Deen et al., 2015; Heine et al., 2015; Kanjlia et al., 2016; Kanjlia et al., 2021; Lane et al., 2015; Liu et al., 2007; Sen et al., 2022; Striem-Amit et al., 2015). We also examined changes in connectivity lateralization—that is, the balance of between versus within hemisphere connectivity, since prior task-based studies have found laterality changes in blindness as well as co-lateralization of occipital and non-occipital networks in this population (Kanjlia et al., 2021; Lane et al., 2017; Tian et al., 2023).

To preview the results, we find that, in infants, the long-range functional connectivity profile of secondary visual areas resembles that of blind adults, whereas V1 falls between blind and sighted adult populations. Relative to sighted adults, both blind adults and infants show stronger coupling between visual cortices and PFC and weaker coupling between visual cortices and non-visual sensory-motor networks. This suggests that vision contributes to modifying the balance of connectivity between occipital and non-visual networks after birth. In contrast, connectivity lateralization patterns appear to reflect blindness-related modification.

The present results provide insight into the developmental process of experience-based functional specialization in human cortex. We find independent effects of visual experience and blindness on the development of visual networks. Aspects of the sighted adult connectivity pattern require visual experience. This is particularly striking for secondary visual cortices, where connectivity with non-visual networks in infants resembles blind more than sighted adults. Both in infants and blind adults, secondary occipital areas showed stronger functional connectivity with higher-order prefrontal cortices than with other sensory-motor networks (S1/M1, A1). Consistent with this observation, one previous study with a small sample of infants found strong connectivity between lateral occipital and prefrontal areas, although there was no comparison to blind adults in that study (Barttfeld et al., 2018). In V1, infants fell somewhere in between sighted and blind adults, suggesting an effect both of vision and of blindness on functional connectivity.

The present results reveal the effects of experience on development of functional connectivity between infancy and adulthood, but do not speak to the precise time course of these effects. Infants in the current sample had between 0 and 20 weeks of visual experience. Comparisons across these infants suggest that several weeks of postnatal visual experience is insufficient to produce a sighted adult connectivity profile. The time course of development could be anywhere between a few months and years and could be tested by examining data from children of different ages.

We propose that vision, as well as temporally coordinated multi-modal experiences, contributes to establishing the sighted adult connectivity profile in visual cortices. For example, coordinated visuo-motor activity during development may enhance connectivity between visual and motor networks. Supporting this conjecture, in infants, motor competence and early experience predict coupling between occipital and motor networks (Colomer et al., 2023).

Many questions remain regarding the neurobiological mechanisms underlying experience-based functional connectivity changes and their relationship to anatomical development. Resting-state functional correlations are an indirect measure of both function and anatomy, and differences in these measures are consistent with many possible underlying biological mechanisms. Long-range anatomical connections between brain regions are already present in infants—even prenatally—though they remain immature (Huang et al., 2009; Kostović et al., 2021; Kostović et al., 2019; Takahashi et al., 2012; Vasung et al., 2017). Functional connectivity changes may stem from local synaptic modifications within these stable structural pathways, consistent with findings that functional connectivity can vary independently of structural connection strength (Fotiadis et al., 2024). Moreover, functional connectivity has been shown to outperform structural connectivity in predicting individual behavioral differences, suggesting that experience-based functional changes may reflect finer-scale synaptic or network-level modulations not captured by macrostructural measures (Ooi et al., 2022). Prior studies also suggest that, even in adults, coordinated sensory-motor experience can lead to enhancement of functional connectivity across sensory-motor systems, indicating that large-scale changes in functional connectivity do not necessarily require corresponding changes in anatomical connectivity (Guerra-Carrillo et al., 2014; Li et al., 2018). Resting-state functional connectivity captures synchrony in blood oxygen level-dependent (BOLD) signal fluctuations rather than causal interactions, and differences in functional connectivity cannot on their own reveal how underlying neurophysiological mechanisms are modified. Connectivity changes between two areas could be mediated by ‘third-party’ hub regions. For example, posterior parietal cortex serves as a cortical hub for multisensory integration and visuo-motor coordination and could mediate occipital-to-sensory-motor communication (Rolls et al., 2023; Sereno and Huang, 2014). Subcortical structures such as the thalamus could also play a mediating role (Vega-Zuniga et al., 2025). Future studies will be needed to determine whether these functional changes are accompanied by alterations in structural connectivity and to probe causal interactions and mechanistic underpinnings.

The current findings reveal both effects of vision and effects of blindness on the functional connectivity patterns of the visual cortex. A further open question is whether visual experience plays an instructive or permissive role in shaping neural connectivity patterns. An instructive role implies that sensory experiences or patterns of neural activity directly shape and organize neural circuitry. In contrast, a permissive role implies that sensory experience or neural activity merely facilitates the influence of other factors—such as molecular signals—on the formation and organization of neural circuits (Crair, 1999; Sur et al., 1999). Studies with animals that manipulate the pattern or informational content of neural activity while keeping overall activity levels constant could distinguish between these hypotheses (Crair, 1999; Roy et al., 2020; Stellwagen and Shatz, 2002). In humans, such manipulations are not feasible, leaving us to study only the consequences of the presence or absence of vision. Under an instructive account, visual and multisensory experience could strengthen coupling between visual and other non-visual sensory-motor cortices through coordinated activity, thereby establishing the sighted adult connectivity pattern. In the absence of visual input, by contrast, the lack of such coordinated activity may prevent these couplings from being established. Alternatively, vision may act permissively, indirectly enabling maturational processes that shift connectivity toward the sighted adult configuration.

A further key question concerns the behavioral relevance of the connectivity signatures observed in the current study. The capacity of occipital cortices to support visual and multimodal behavior in sighted people may depend not only on local visual cortex function but also on the capacity of the visual system to coordinate its function with non-visual networks. Does enhanced connectivity between visual and non-visual sensory-motor networks facilitate multimodal integration for sighted people, for example, when catching a ball? Potentially consistent with this possibility, recent evidence suggests that people who grew up blind but recover sight in adulthood show multimodal integration deficits (Badde et al., 2020; Guerreiro et al., 2015; Mowad et al., 2020; Putzar et al., 2007) and distinct occipital oscillations (Pant et al., 2023).

Conversely, for people who remain blind throughout life, visual-PFC connectivity could enable recruitment of visual cortices for higher-order non-visual functions, such as language and executive control (Bedny et al., 2011; Kanjlia et al., 2021). Our results suggest that the pattern of connectivity observed in blind adults may build on connectivity patterns already present in infancy: like blind adults, infants show stronger occipital–PFC than occipital–sensory–motor coupling. Repeated engagement of occipital networks during higher-cognitive tasks in early development could further enhance connectivity and enable specialization of visual networks for different non-visual higher-order functions.

Some prior studies have measured resting-state and task-based functional profiles in the same participants. These studies find that within visual cortices of blind people, the task-based profile of a cortical area is related to its resting-state connectivity pattern (Abboud and Cohen, 2019; Deen et al., 2015; Kanjlia et al., 2016; Kanjlia et al., 2021). This suggests that these two measures are related. However, the time course of this relationship, the developmental trajectory and mechanism of plasticity is not known. Primarily, this is because there is very little relevant developmental evidence. For example, in the current study, we find that the resting-state profile of secondary visual networks in infants is similar to that of blind adults. However, we do not know whether the visual cortices of infants show enhanced task-based cross-modal responses, relative to sighted adults, and how this compares to responses observed in blind adults. Future work with infants and children would be able to address this question.

In the current study, the clearest evidence for functional change driven by blindness was observed for laterality. Connectivity lateralization in sighted infants resembles that of sighted adults, in both V1 and secondary visual cortices. Relative to both sighted infants and sighted adults, blind adults show more lateralized connectivity patterns between occipital and prefrontal cortices. Previous studies suggest that in people born blind, occipital and non-occipital language responses are co-lateralized (Lane et al., 2017; Tian et al., 2023). We speculate that habitual activation of visual cortices by higher-cognitive tasks, such as language, which are themselves highly lateralized, contributes to this biased connectivity pattern of occipital cortex in blindness. Taken together, these results suggest a developmental framework in which intrinsic connectivity present in infancy provides a scaffold that is subsequently shaped and reinforced by experience-dependent recruitment, through either visual experience or the lifelong absence of vision in blindness. Longitudinal work across successive developmental stages will be crucial to test how the alternative trajectories shaped by visual experience versus blindness unfold over development.

Neonate data were from the third release of the Developing Human Connectome Project (https://www.developingconnectome.org). The de-identified blind and sighted adults' data were posted on openICPSR (https://doi.org/10.3886/E198832V1).

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Author details

1. Mengyu Tian

   1. Center for Educational Science and Technology, Beijing Normal University, Zhuhai, China
   2. Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, United States

   Contribution

   Conceptualization, Data curation, Formal analysis, Visualization, Writing – original draft, Writing – review and editing

   For correspondence

   mengyutian@jhu.edu

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2289-4415

2. Xiang Xiao

   Department of Psychology, Faculty of Art and Science, Beijing Normal University at Zhuhai, Zhuhai, China

   Contribution

   Data curation, Software, Formal analysis, Visualization, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2266-4284

3. Huiqing Hu

   Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin, Ireland

   Contribution

   Software, Methodology

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5652-9606

4. Rhodri Cusack

   Trinity College Institute of Neuroscience and School of Psychology, Trinity College Dublin, Dublin, Ireland

   Contribution

   Supervision, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-5234-7415

5. Marina Bedny

   Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, United States

   Contribution

   Conceptualization, Supervision, Funding acquisition, Writing – original draft, Writing – review and editing

   Competing interests

   No competing interests declared

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