Subclinical variability in visual function modulates visual dependence - independent of age

Our main findings were that healthy young and older adults had similar SVV tilt error, and thus visual dependence. However, visual acuity and contrast sensitivity, which were observed to be lower in the older adults, were associated with greater SVV tilt error. ACME analysis identified significant modulation of SVV tilt error via age-related declines in both visual acuity and contrast sensitivity. In contrast, depth perception and lower peripheral vision did not differ between the groups. Depth perception, however, had a small but significant negative relationship with SVV. Vision-related health and quality of life (VFQ-25) were similar in each group, although higher VFQ-25 scores were associated with better visual acuity. Young adults reported higher RDT-induced vection, however, there were no differences in nausea, VMSQ or MSSQ scores between the groups.

Decline in visual function with age

The observation of lower visual acuity and contrast sensitivity in older adults is consistent with previous research (Saftari and Kwon 2018b, a). Notably, our cohort possessed clinically good (corrected or habitual) visual acuity (LogMAR < 0.3). The finding that depth perception did not decline with age is consistent with prior research (Norman et al. 2008). However, whilst we employed the classical Howard-Dolman apparatus method, there are other more modern techniques such as the Randot test (Wang et al. 2010).

In contrast to previous research, we did not observe an age-related decline in lower peripheral vision (Ramrattan et al. 2001). This failure may relate to the fact that our participants, regardless of age, were free from ophthalmological conditions such as glaucoma and macular degeneration, which are associated with peripheral vision loss (Ramrattan et al. 2001). The LPV test in this study, whilst inexpensive and practical, lacked the precision and granularity of automated visual field analysers such as the Goldmann perimetry apparatus (Broadway 2012). As a result, it is possible that subtle declines in the lower visual fields were not detected. Future studies, particularly in healthy adults could benefit from incorporating more sensitive automated perimetry techniques to detect sub-clinical changes in peripheral vision.

Subjective assessment of visual function is associated with ageing

Older adults demonstrated marginally (sub-clinical) lower visual acuity (VA) and contrast sensitivity (CS); however, their self-perceived vision-related health and quality of life were comparable to younger adults. Older adults in our study reported higher VFQ-25 scores (91.6 ± 6.3) compared to those (54.4 ± 21.5) reported by Inoue and colleagues, although their participants (69.6 ± 14.5 yrs) were older than those in our study (62.4 ± 6.7 yrs) (Inoue et al. 2018).

Additionally, our participants were healthy, physically (albeit not formally assessed) and socio-economically active, and free from major co-morbidities and ophthalmological pathology. Control of these factors may explain the failure to observe differences in VFQ-25 in our cohort. However, the VFQ-25 may be a useful proxy instrument in those with low level, but functionally significant visual pathology – although an issue may be that older adults may recalibrate expectation and satisfaction (Cho and Cheon 2023). In future, concurrent assessment of other perceptual domains associated with vestibular and/or proprioceptive pathology may be warranted.

No association between visual dependence and ageing

In our study, age was not an independent predictor of SVV tilt error. This finding contrasts with previous research, which attribute increased visual dependence to age-related declines in non-visual sensory and sensorimotor function (Osoba et al. 2019b). In fact, SVV tilt error was comparable between our older and younger adults. This is consistent with that reported by Lee (Lee 2017), who (albeit in a small sample) also observed significant inter-observer variability in SVV tilt error among older adults.

In contrast, Agathos and colleagues (Agathos et al. 2015a), reported an age-related increase in SVV tilt error (+ 4.9 ± 2.0 degrees) in a cohort of twenty older adults. This cohort was larger than our older adult group (n = 12) but also critically it was significantly older (74.1 ± 3.7 vs. 62.4 ± 6.7 years). Thus, our group is likely to present less significant multi-systems degradation.

Furthermore, we recruited healthy individuals with active lifestyles, as older adults who remain physically active exhibit superior proprioceptive (Ribeiro and Oliveira 2007), vestibular (Wiszomirska et al. 2015), and cognitive function (Xu et al. 2023) with age. Given higher levels of visual dependence in older adults is proposed to result from impaired sensory and/or sensorimotor function, it is plausible that in addition to accounting for differences between cohorts, physical activity levels in older adults may relate to intra-individual variation in visual dependence in older adults – both reflecting and driving MSI.

Unfortunately, we were unable to quantify habitual physical activity or relevant cognitive function (Green et al. 2010). However, older active ex-tennis professionals have previously demonstrated lower visual dependence than sedentary controls (Rotella and Bunker 1978). Thus, evaluation of activity as a co-factor with sensory function and their association with visual dependence in older adults warrants further study.

Increased visual dependence is associated with clinically insignificant visual function deficits

Multiple regression modelling identified sub-clinical variability in visual acuity as the primary predictor of SVV tilt error variability, whilst depth perception demonstrated a small but significant (negative) relationship with SVV. Contrast sensitivity was also associated with increased SVV tilt error, although only at the univariate level. Agathos and colleagues (Agathos and Shanidze 2024) reported correlations between visual acuity, contrast sensitivity and SVV tilt error in individuals with central field loss - noting that contrast sensitivity had a stronger association.

One potential explanation for the fact that in our study visual acuity was the stronger predictor is that whilst contrast sensitivity levels were similar between the two studies (1.43 ± 0.26 vs. 1.51 ± 0.16; 94.7% agreement; Cohen’s d = 0.81), visual acuity (LogMAR) was significantly reduced in Agathos’s study (0.80 ± 0.60 vs. 0.07 ± 0.13; 8.7% agreement; Cohen’s d = -1.90) – reflective of their CFL.

Whilst there was no direct effect of ageing on visual dependence, ACME analysis indicates that the association between visual dependence, and both lower visual acuity and contrast sensitivity represents an indirect corollary of ageing. The paradox of why some older adults rely on visual information, despite declining visual function is unresolved. However, significant SVV tilt error inter-individual variability suggests that whilst visual signal processing is important – there are likely to be a range of factors (Osoba et al. 2019a) that contribute to the tendency to prioritise visual signals. Thus, subsequent studies should seek to quantify multi-sensory function (including visual, vestibular and proprioceptive), cognitive function, perception of function and falls risk along with physical activity in healthy and unisensory pathological groups to ascertain inter-relationships via ACME analysis.

On potential issue with the use of the RDT to sensitively assess visual dependence is its dependence upon having sufficient visual fidelity to not differently affect the assessment of the fluorescent rod position, and thus tilt. Despite this issue the test has been used even with visual pathology (Agathos and Shanidze 2024). In our study, since most participants demonstrated normal visual acuity (The Royal College of Ophthalmologists 2021), it is unlikely that sub-clinically ‘lower’ vision limited their performance. However, subsequent studies evaluating a greater range of visual fidelity, to confirm that this was not a limiting factor, should be performed by calculating the angular separation of adjacent dots within the RDT interface. Such data may even warrant being a feature of RDT testing. Additionally, comparisons with other methods of visual dependence testing (e.g., VIRVEST (Totilienė et al. 2021) warrant consideration.

Vision, visual dependence, and the law of inverse effectiveness

The observation that lower sub-clinical visual function (visual acuity and contrast sensitivity) was associated with increased SVV tilt error and hence visual dependence, challenges the sensory reweighting theory (Peterka 2002), which describes the downregulation of lower fidelity sensory signals, and upweighting of higher fidelity signals. The design of the RDT test attempted to minimize vestibular and proprioceptive feedback, however, they may have still played a role – particularly as our participants were recruited with no evident sensory dysfunction. Whether the prioritisation of ‘poorer’ visual afferents is concurrent with the relative degradation of vestibular and proprioceptive signals, warrants further study.

Alternatively, the ‘law of inverse effectiveness’ (Stevenson et al. 2012), posits that multisensory integration is more effective when individual sensory inputs are weak or ambiguous. Thus, by minimising vestibular and proprioceptive feedback we may exaggerate visual dependence. Whilst this is a trade-off, this approach was more ecological than Romberg testing with eyes closed (Black et al. 1982).

Increased vection is associated greater visual dependence

Higher SVV tilt error was associated with higher vection rating consistent with previous studies (Pavlou et al. 2011). However, were no differences in RDT-induced nausea, VMSQ scores, or susceptibility to motion sickness between younger and older adults. Vection did not relate to any visual function parameters, but further exploration is warranted with groups with higher motion sickness susceptibility – which was low in our groups. This low susceptibility also accounts for the absence, or only low levels nausea in response to the RFT.

Interestingly, susceptibility to motion sickness was associated with better lower peripheral vision – which itself was similar in each group. Peripheral vision is crucial for detecting motion and maintaining spatial orientation. The independent findings of higher vection scores in visually dependent individuals, and increased susceptibility to motion sickness in individuals with better lower peripheral vision, may indicate a greater reliance on peripheral visual cues for orientation. Despite there being no interaction between visual acuity, contrast sensitivity and lower peripheral vision in this study, it is plausible, as suggested by Agathos and colleagues (Agathos and Shanidze 2024), that in individuals with poorer central field vision, peripheral visual cues become more pertinent for spatial orientation. Whether these findings persist in larger cohorts require studies with differential visual fidelities within the clinical, and as in this study the sub-clinical range, along with physical activity levels, given that visual impairment is associated with limitation of physical activity and fear of falling(Nguyen et al. 2015).

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