A VEP investigation of parallel visual pathway development in primary school age children

Different features of visual function mature along unique timescales through infancy and early childhood. It is not clear which functions continue to mature in school age children. Functions believed to be mediated by the Magnocellular (M) and
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   Documenta Ophthalmologica  99:  1–10, 1999.© 2000  Kluwer Acadeic Publishers. Printed in the Netherlands. A VEP investigation of parallel visual pathwaydevelopment in primary school age children GAEL E. GORDON 1 , 2 and DAPHNE L. McCULLOCH 11  Department of Psychology, Fylde College, Lancaster University, Lancaster, LA1 4YF, UK; 2  Department of Vision Sciences, Glasgow Caledonian University, Glasgow, UK  Accepted 4 July 1999 Abstract.  Different features of visual function mature along unique timescales through in-fancy and early childhood. It is not clear which functions continue to mature in school agechildren. Functions believed to be mediated by the Magnocellular (M) and Parvocellular (P)pathways were compared in five- ( n =25), eight- ( n =21) and eleven-year-old children ( n =21)and young adult controls ( n =20). Steady-state visual evoked potentials were recorded fromoccipital electrodes in response to very low spatial frequency gratings, at a series of contrasts(M), and to high contrast gratings at a series of spatial frequencies (P). No evidence wasfound to indicate M pathway development across these age groups. However, the youngestchildren demonstrated elevated VEP thresholds to the high contrast gratings compared witheither the adults or eleven-year-olds. This difference in threshold implies an immaturity of thehigh contrast, high spatial frequency stream, i.e. the putative P pathway. Key words:  magnocellular pathway, parvocellular pathway, steady state VEP, visual develop-ment Abbreviations:  IQR – inter-quartile range; SNR – signal to noise ratio Introduction The human visual system is not fully developed by the age of five (e.g. [1–3]). Interestingly, different aspects of visual function appear to develop alongunique timescales. For example, while the peak latencies of transient VEP inresponse to low spatial frequencies is adult-like by the age of two [4, 5], thepeak latencies in response to high contrast, high spatial frequency patternscontinues to reduce through childhood [6], possibly until early puberty [7].Infant sensitivity to fast flicker also apparently develops in advance of sens-itivity to slow temporal frequency flicker [8–10]. This is mirrored in infantsensitivity to measures of motion detection: responses are relatively less welldeveloped for slow velocities compared to those for higher velocity stimuli ininfants [11–14].  2Such a dichotomy points to independent developmental rates for at leasttwo underlying visual pathways. The main candidates for this would appearto be the magnocellular (M) and parvocellular (P) pathways. The M pathwayis believed to be primarily responsible for the mediation of information re-garding high temporal frequency, low spatial frequency and very low contrasttargets; the P pathway is thought to be the main carrier of high contrast, colorand high spatial frequency information, especially at lower temporal frequen-cies (see [15] for a review). There is some anatomical evidence to supportthe hypothesis that the M pathway develops in advance of the P pathway. Ithas been found, for example, that horizontal connections in layer 4B of theprimary visual cortex, which processes inputs from the M pathway, are adult-like in appearance by about eight weeks post-natal age; similar connectionsin layers two and three, which process form and color (P inputs), continueto mature until 15 months of age [16, 17]. However, a recent study [18] hasreported finding continued development of a VEP component that may bedriven by the M pathway at least until 11 years of age.The aim of the present study was to investigate directly, using VEPswhether children with presumed normal visual development show any devel-opment in the putative parallel pathways the primary school years. Subjects Subjects were recruited at random from amongst the children who had passeda vision screening at their school. The school has a roll of 423 children andis the sole provider of primary education for a small market town and itssurrounding rural area. The vision screening was conducted by two optomet-rists (one of the authors and one other). A child was deemed to have failedthe screening if their vision was reduced (a logMAR score of 0.2 or less)or unequal (a difference 0.2 or more log units) or if there was any evidenceof abnormal binocular development (e.g. strabismus). The children were re-cruited in three age groups: five- ( n =25; mean age 5 years 6.96 months, sd3.13 months), eight- ( n =21; mean age 8 years, 2.65 months, sd 3.13 months)and eleven-year-olds ( n =21; mean age 11 years 5.00 months, sd 3 months).These age groups were chosen to cover as wide an age span as possible.Permission was sought and granted from the Department of Education,Grampian Regional Council to approach parents at the school. Informed con-sent was received from the parents to record VEPs from all those childrenwho had taken part in the vision screening.  3 Methods VEPs were measured using the Enfant 4010 system (NeuroScientific Corp.,Farmingdale, NY) running on a Dell Dimension XPS 466V computer. Thesystem consists of a PixelLink high resolution 17 ′′ color monitor (60 Hzrefresh rate) triggered by the microcomputer. The signals from each elec-trode were amplified 10,000 fold and were recorded with a bandpass filter setbetween 0.5 and 60 Hz using isolated amplifiers (AMP 800, NeuroScientificCorp.).Subject’s head circumferences and nasion to inion measurements wererecorded. Recordings of steady state VEPs were made from Oz, 03 and 04on the occipital scalp [19]. The reference electrode was placed on the frontalscalp (Fz) and the earth on the crown of the head (Cz). Impedance for eachelectrode site was below 5 k   . The space average luminance of the stimulusscreen was 56.3 cd/m 2 . The screen subtended 19 by 25 degrees at the testdistance. Subjects were asked tofixate the centre of the screen for the durationof the testing session.All stimuli presented to test primarily the M pathway were horizontal grat-ings of relatively low contrast. These gratings were sinusoidally modulatedspatially, with aspatial frequency of 0.27 cycles per degree (cpd) and reversedabruptly (temporal square wave) at a temporal frequency of 12 Hz. BinocularVEPs were recorded in all children for at least one trial at three contrasts:20, 10, 5%. In most children, a second trial was recorded. Additional con-trast levels were attempted in co-operative children. Stimuli presented to testthe P pathway were high contrast (80%), horizontal, sinusoidal gratings of high spatial frequencies. These gratings were reversed abruptly at a temporalfrequency of 6 Hz. VEPs were recorded in all children for at least one trialat three spatial frequencies: 3.75, 7.5, 15 cpd. All trials were presented ina pseudo-randomised order. Children with a refractive correction wore theirspectacles during the test.Discrete Fourier Transforms were performed on averaged steady-stateVEPs obtained at Oz. A signal-to-noise ratio (SNR) was calculated by di-viding the amplitude of the component of the Discrete Fourier Transformsat the reversal rate (i.e. twice the temporal frequency) by an averaged noiseestimate. Noise values were obtained for each trial by averaging, off-line,five noise bins on either side of the frequency of interest, 1 Hz away fromthat frequency to avoid the noise being contaminated by signal spread [20].MANOVAs were performed on the outputted data for both groups. One po-tential problem with this form of analysis is that it may not be true to say,simply because one individual has a larger SNR than another, that they cannecessarily ‘see’ a stimulus better. We therefore conducted further analyses  4 Figure 1.  Mean SNRs ( ± se) plotted for three spatial frequency levels for the four age groups.The five- and eight-year-olds had significantly smaller SNRs compared to the adults andeleven-year-olds in response to the 7.5 cpd grating (indicated by the asterisk; p< 0.05). on the data after classifying the SNR from each trial as significantly aboveor below threshold. The threshold criteria were calculated for the presentconfiguration using Albersheim’s detection equation [21]. This is an accurateapproximation to the Robertson detection curves which have been previouslyapplied to the analysis of steady-state VEP amplitudes [22]. Chi Square testswere then executed on the resultant ‘pass/fail’ data. Results Success rates All the children completed one trial at each of the 3.75, 7.5 and 15 cpd spatialfrequency levels. All the eight- and eleven-year-old children also completedthe 10 and 12 cpd level, along with 18 (72%) of the five-year-olds. Noneof the five-year-olds completed the 20 cpd spatial frequency trial, however18 (85.7%) of the eight-year-olds, and 20 (95.2%) of the eleven-year-oldshad a VEP recorded at this spatial frequency. VEPs were also recorded fortwo trials each of 5, 10 and 20% contrast gratings, for all except three five-year-olds and two eleven-year-olds of whom one trial only was recorded. Anadditional recording of the VEP in response to the 7% contrast grating wasonly achieved in four of the five-year-old subjects, however 12 of the eight-year-olds and 16 of the 11-year-olds had VEPs recorded for one trial of thisstimulus and a 9% contrast grating.  5 Table 1.  SNRs for high contrast (P) stimuliSpat Frq 5-yr-olds 8-yr-olds 11-yr-olds Adults(cpd) Median SNR Median SNR Median SNR Median SNR(IQR) (IQR) (IQR) (IQR)3.75 3.63 (2.28) 2.91 (4.43) 3.30 (3.57) 5.15 (4.08)7.5 2.23 (2.05) 1.93 (3.29) 4.75 (5.93) 5.31 (5.77)10 2.88 (1.81) 2.74 (2.71) 3.16 (2.44) 3.52 (4.47)12 1.70 (1.81) 2.79 (1.89) 3.03 (3.10) 3.18 (2.16)15 1.96 (1.08) 2.59 (2.00) 2.12 (3.13) 2.63 (1.45)20 – 1.57 (0.68) 2.15 (1.31) 1.72 (0.99) P stimuli Two-way repeated measures ANOVA was performed on the computed SNRs.Significant effects of age and spatial frequency were found ( p < 0.05). Post-hoc Dunnet- t   test indicated the age effect was due to lower SNRs in thefive-year-olds at the 7.5 cpd stimulus. The mean SNRs for large (3.75 cpd),intermediate (7.5 cpd) and small (15 cpd) gratings for the four groups areplotted in Figure 1.The SNRs were classed as significant or not-significant by Albersheim’sdetection equation. Chi-squared tests were performed on the groups at eachspatial frequency level to compare the proportions of significant signals.The adults and eleven-year-olds had proportionally more significant SNRsfor the 7.5 cpd stimulus than either of the two younger groups of children(Chi-square test, p < 0.05). The eleven-year-olds were not different from theadults for this spatial frequency (Chi-square test,  p > 0.1). The four groupswere not different from each other for the 3.75, 10 or 15 cpd stimulus level(Chi-square test,  p > 0.1). Although a significant VEP was recorded in re-sponse to the 12 cpd stimulus for fewer five-year-olds (47.1% of five-year-olds compared with 81.0% of eight-year-olds and 62.0% of eleven-year-olds),this difference was not statistically significant (Chi-square test, p > 0.1). Asnone of the five-year-olds completed a 20 cpd trial, the remaining two groupswere compared with the adults and no difference was found (Chi-square test, p > 0.1). The SNRs for each spatial frequency were not normally distrib-uted but were positively skewed. Median SNRs (and inter-quartile ranges)for each spatial frequency and for each age group are presented alongside thecorresponding adult values in Table 1.Further analysis was considered necessary to test whether the proportionof significant SSVEPs reduced with increasing spatial frequency for the chil-
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