Documenta Ophthalmologica

, Volume 118, Issue 2, pp 109–119 | Cite as

Maturation of steady-state flicker VEPs in infants: fundamental and harmonic temporal response frequencies

  • C. Pieh
  • D. L. McCulloch
  • U. Shahani
  • H. Mactier
  • M. Bach
Original Research Article

Abstract

Transient flash VEPs allow objective assessment of visual function and are easily recorded in young infants. However, due to their high variability, they are an insensitive surrogate marker of visual development. The aim of our study was to investigate the early maturation of temporal characteristics of steady-state flicker VEPs. Data from 53 VEP sessions were analyzed in term-born infants between birth and 20 months of age. The stimulus was a square-wave modulated luminance flicker with 80% modulation depth at temporal frequencies of 4.7, 7.5, 12.5, and 19 Hz. A total of 18 healthy adults aged between 21 and 54 years served as controls. Contingent on the stimulus frequency, we found pronounced changes of the flicker VEP with age. Regression lines fit to the first harmonic VEP magnitude as a function of age between 3 and 88 weeks of age indicated increases at 7.5 (P = 0.004), 12.5 (P < 0.001), and 19 Hz (P = 0.07) and a non-significant decrease at 4.7 Hz (P = 0.3). The magnitude of the second harmonic increased for all frequencies (4.7 (P = 0.05), 7.5 (P = 0.01), 12.5 (P = 0.13), and 19 Hz (P = 0.18)). Over the whole infant age range, the flicker VEP was dominated by the first harmonic, in contrast to adults, where the response was typically shifted to a higher harmonic at low stimulus frequencies. The optimal stimulus frequency, defined as the frequency eliciting the highest magnitude for F1, shifted to higher rates with age. Due to the difference from adult responses, further developmental changes of the temporal properties must be assumed to occur after the age of 20 months. Changes in temporal characteristics of the flicker VEP with age may be useful as an indicator of visual system maturation and a useful tool to detect visual delay.

Keywords

Flicker VEP Infant Maturation Temporal frequency 

Notes

Acknowledgements

We thank the parents and infants who volunteered their time for this study. Dr Christina Pieh was supported by the Royal Society of Edinburgh - International Exchange Visitor Programme. We are grateful to Dr Michael Bradnam and Richard Boulton for supporting the data analysis in Glasgow and to Richard Boulton and Leslie Farrell for assisting with data collection.

References

  1. 1.
    Apkarian P (1993) Temporal frequency responsivity shows multiple maturational phases: state-dependent visual evoked potential luminance flicker fusion from birth to 9 months. Vis Neurosci 10:1007–1018PubMedCrossRefGoogle Scholar
  2. 2.
    Apkarian P, Mirmiran M, Tijssen R (1991) Effects of behavioural state on visual processing in neonates. Neuropediatrics 22:85–91PubMedCrossRefGoogle Scholar
  3. 3.
    Banks MS, Salapatek P (1978) Acuity and contrast sensitivity in 1-, 2-, and 3-month-old human infants. Invest Ophthalmol Vis Sci 17:361–365PubMedGoogle Scholar
  4. 4.
    Barnet AB, Friedman SL, Weiss IP, Ohlrich ES, Shanks B, Lodge A (1980) VEP development in infancy and early childhood. A longitudinal study. Electroencephalogr Clin Neurophysiol 49:476–489. doi:10.1016/0013-4694(80)90390-9 PubMedCrossRefGoogle Scholar
  5. 5.
    Birch EE, Gwiazda J, Bauer JA Jr, Naegele J, Held R (1983) Visual acuity and its meridional variations in children aged 7–60 months. Vision Res 23:1019–1024. doi:10.1016/0042-6989(83)90012-3 PubMedCrossRefGoogle Scholar
  6. 6.
    Bobon DP, Lecoq A, von Frenckell R, Mormont I, Lavergne G, Lottin T (1982) Critical flicker fusion frequency in psychopathology and psychopharmacology. Review of the literature. Acta Psychiatr Belg 82:7–112PubMedGoogle Scholar
  7. 7.
    Crognale MA, Kelly JP, Chang S, Weiss AH, Teller DY (1997) Development of pattern visual evoked potentials: longitudinal measurements in human infants. Optom Vis Sci 74:808–815. doi:10.1097/00006324-199710000-00020 PubMedCrossRefGoogle Scholar
  8. 8.
    Dannemiller JL, Banks MS (1983) The development of light adaptation in human infants. Vision Res 23:599–609. doi:10.1016/0042-6989(83)90065-2 PubMedCrossRefGoogle Scholar
  9. 9.
    de Courten C, Garey LJ (1982) Morphology of the neurons in the human lateral geniculate nucleus and their normal development. A Golgi study. Exp Brain Res 47:159–171. doi:10.1007/BF00239375 PubMedCrossRefGoogle Scholar
  10. 10.
    de Monasterio FM (1978) Properties of ganglion cells with atypical receptive-field organization in retina of macaques. J Neurophysiol 41:1435–1449PubMedGoogle Scholar
  11. 11.
    De Valois RL, De Valois KK (1988) Spatial vision. Oxford Univ Press, New YorkGoogle Scholar
  12. 12.
    De Vries-Khoe LH, Spekreijse H (1982) Maturation of luminance and pattern EPs in man. In: Niemeyer G, Ch Huber (eds) Techniques in clinical electrophysiology of vision. Doc Ophthalmol Proc Ser, Vol 31. Dr W Junk, The Hague, pp 461–475Google Scholar
  13. 13.
    Ellingson RJ (1986) Development of visual evoked potentials and photic driving responses in normal full term, low risk premature, and Trisomy-21 infants during the first year of life. Electroencephalogr Clin Neurophysiol 63:309–316. doi:10.1016/0013-4694(86)90015-5 PubMedCrossRefGoogle Scholar
  14. 14.
    Garey LJ, de Courten C (1983) Structural development of the lateral geniculate nucleus and visual cortex in monkey and man. Behav Brain Res 10:3–13. doi:10.1016/0166-4328(83)90145-6 PubMedCrossRefGoogle Scholar
  15. 15.
    Hendrickson AE, Yuodelis C (1984) The morphological development of the human fovea. Ophthalmology 91:603–612PubMedGoogle Scholar
  16. 16.
    Herschkowitz N (1988) Brain development in the fetus, neonate and infant. Biol Neonate 54:1–19PubMedCrossRefGoogle Scholar
  17. 17.
    Hickey TL, Spear PD, Kratz KE (1977) Quantitative studies of cell size in the cat’s dorsal lateral geniculate nucleus following visual deprivation. J Comp Neurol 172:265–281. doi:10.1002/cne.901720206 PubMedCrossRefGoogle Scholar
  18. 18.
    Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  19. 19.
    Horsten GP, Winkelman JE (1960) Development of the ERG in relation to histological differentiation of the retina in man and animals. Arch Ophthalmol 63:232–242PubMedGoogle Scholar
  20. 20.
    Hubel DH, Wiesel TN (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 160:106–154PubMedGoogle Scholar
  21. 21.
    Huttenlocher PR (1970) Myelination and the development of function in immature pyramidal tract. Exp Neurol 29:405–415. doi:10.1016/0014-4886(70)90068-3 PubMedCrossRefGoogle Scholar
  22. 22.
    Huttenlocher PR, De Courten C, Garey LJ, Van der Loos H (1982) Synaptic development in human cerebral cortex. Int J Neurol 16–17:144–154Google Scholar
  23. 23.
    Kraemer M, Abrahamsson M, Sjostrom A (1999) The neonatal development of the light flash visual evoked potential. Doc Ophthalmol 99:21–39. doi:10.1023/A:1002414803226 PubMedCrossRefGoogle Scholar
  24. 24.
    Mackie RT, McCulloch DL (1995) Assessment of visual acuity in multiply handicapped children. Br J Ophthalmol 79:290–296. doi:10.1136/bjo.79.3.290 PubMedCrossRefGoogle Scholar
  25. 25.
    Magoon EH, Robb RM (1981) Development of myelin in human optic nerve and tract. A light and electron microscopic study. Arch Ophthalmol 99:655–659PubMedGoogle Scholar
  26. 26.
    Mayer DL, Dobson V (1982) Visual acuity development in infants and young children, as assessed by operant preferential looking. Vision Res 22:1141–1151. doi:10.1016/0042-6989(82)90079-7 PubMedCrossRefGoogle Scholar
  27. 27.
    McCulloch DL, Skarf B (1991) Development of the human visual system: monocular and binocular pattern VEP latency. Invest Ophthalmol Vis Sci 32:2372–2381PubMedGoogle Scholar
  28. 28.
    McCulloch DL, Taylor MJ, Whyte HE (1991) Visual evoked potentials and visual prognosis following perinatal asphyxia. Arch Ophthalmol 109:229–233PubMedGoogle Scholar
  29. 29.
    Meigen T, Bach M (1999) On the statistical significance of electrophysiological steady-state responses. Doc Ophthalmol 98:207–232. doi:10.1023/A:1002097208337 PubMedCrossRefGoogle Scholar
  30. 30.
    Moskowitz A, Sokol S (1983) Developmental changes in the human visual system as reflected by the latency of the pattern reversal VEP. Electroencephalogr Clin Neurophysiol 56:1–15. doi:10.1016/0013-4694(83)90002-0 PubMedCrossRefGoogle Scholar
  31. 31.
    Nakayama K (1966) Studies on the human optic nerve, especially its myelinization. Nippon Ganka Gakkai Zasshi 70:1511–1525PubMedGoogle Scholar
  32. 32.
    Orel-Bixler D, Haegerstrom-Portnoy G, Hall A (1989) Visual assessment of the multiply handicapped patient. Optom Vis Sci 66:530–536. doi:10.1097/00006324-198908000-00007 PubMedCrossRefGoogle Scholar
  33. 33.
    Pike AA, Marlow N (2000) The role of cortical evoked responses in predicting neuromotor outcome in very preterm infants. Early Hum Dev 57:123–135. doi:10.1016/S0378-3782(99)00061-4 PubMedCrossRefGoogle Scholar
  34. 34.
    Regal DM (1981) Development of Critical flicker frequency in human infants. Vision Res 21:549–555. doi:10.1016/0042-6989(81)90100-0 PubMedCrossRefGoogle Scholar
  35. 35.
    Regan D (1989) Visual evoked potentials to luminance changes. Elsevier Science Publishing, New YorkGoogle Scholar
  36. 36.
    Shepherd A, Saunders K, McCulloch D (1999) Effect of sleep state on the flash visual evoked potential. A case study. Doc Ophthalmol 98:247–256. doi:10.1023/A:1002471022790 PubMedCrossRefGoogle Scholar
  37. 37.
    Shepherd AJ, Saunders KJ, McCulloch DL, Dutton GN (1999) Prognostic value of flash visual evoked potentials in preterm infants. Dev Med Child Neurol 41:9–15. doi:10.1017/S0012162299000031 PubMedCrossRefGoogle Scholar
  38. 38.
    Taravella CL, Clark G (1963) Discrimination of intermittent photic stimulation in normal and brain-damaged cats. Exp Neurol 7:282–293. doi:10.1016/0014-4886(63)90075-X PubMedCrossRefGoogle Scholar
  39. 39.
    Taylor MJ, McCulloch DL (1991) Prognostic value of VEPs in young children with acute onset of cortical blindness. Pediatr Neurol 7:111–115. doi:10.1016/0887-8994(91)90006-7 PubMedCrossRefGoogle Scholar
  40. 40.
    Taylor MJ, McCulloch DL (1992) Visual evoked potentials in infants and children. J Clin Neurophysiol 9:357–372. doi:10.1097/00004691-199207010-00004 PubMedCrossRefGoogle Scholar
  41. 41.
    Taylor MJ, Menzies R, MacMillan LJ, Whyte HE (1987) VEPs in normal full-term and premature neonates: longitudinal versus cross-sectional data. Electroencephalogr Clin Neurophysiol 68:20–27. doi:10.1016/0168-5597(87)90066-9 PubMedCrossRefGoogle Scholar
  42. 42.
    Vitova Z, Hrbek A (1972) Developmental study on the responsiveness of the human brain to flicker stimulation. Dev Med Child Neurol 14:476–486PubMedGoogle Scholar
  43. 43.
    Yuodelis C, Hendrickson A (1986) A qualitative and quantitative analysis of the human fovea during development. Vision Res 26:847–855. doi:10.1016/0042-6989(86)90143-4 PubMedCrossRefGoogle Scholar
  44. 44.
    Zrenner E (1983) Neurophysiological aspects of color vision in primates. Springer-Verlag, BerlinGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • C. Pieh
    • 1
  • D. L. McCulloch
    • 2
  • U. Shahani
    • 2
  • H. Mactier
    • 3
  • M. Bach
    • 1
  1. 1.University Eye Clinic, University of FreiburgFreiburgGermany
  2. 2.Vision SciencesGlasgow Caledonian UniversityGlasgowUK
  3. 3.Neonatal UnitPrincess Royal Maternity and University of GlasgowGlasgowUK

Personalised recommendations