Skip to main content

Advertisement

SpringerLink
Log in

Human vision with a lesion of the parvocellular pathway: an optic neuritis model for selective contrast sensitivity deficits with severe loss of midget ganglion cell function

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Achromatic visual function in primates is distributed between two pathways from retina to cortex, the parvocellular and the magnocellular. The relative contribution of these to human achromatic vision is controversial and largely unknown. Here, we use an optic neuritis (ON) model to investigate the effects of a severe loss of parvocellular function on human contrast sensitivity. In our first experiment, we use Gabor stimuli (0.5 cpd, 2 Hz) to show that, compared to normal control eyes, ON causes selective deficits in the two chromatic, cone opponent pathways, with L/M cone opponency affected more than S cone opponency, and a relative sparing of achromatic function. Since L/M cone opponency is carried exclusively by the midget ganglion cells of the parvocellular pathway, this demonstrates a selective deficit of parvocellular function. In a second experiment, we report on two subjects who have lost all L/M cone opponent response in both eyes, indicating a severe loss of parvocellular function. We measure the spatial and temporal contrast sensitivity functions of their remaining achromatic vision, compared with a normal control group, to determine the selectivity of the visual deficit caused by the differential parvocellular loss, and assess the relative contributions of the parvocellular and magnocellular pathways to achromatic contrast sensitivity. We find that parvocellular function contributes selectively at mid- to high spatial frequencies (at low temporal frequencies), whereas magnocellular function determines contrast sensitivity over a very broad temporal frequency range (at low spatial frequencies). Our data bear a striking resemblance to results obtained from primate parvocellular lesions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ON:

Optic neuritis

MS:

Multiple sclerosis

L, M and S cones:

Long, medium and short wavelength sensitive cones

P-cells:

Parvocellular cells

M-Cells:

Magnocellular cells

K-cells:

Koniocellular cells

LGN:

Lateral geniculate nucleus of the thalamus

Ach:

Achromatic

RG:

Red-Green

BY:

Blue-Yellow

CPD:

Cycles per degree

AE:

Affected eye

FE:

Unaffected fellow eye

NC:

Normal controls

References

  • Alvarez SL, King-Smith PE (1984) Dichotomy of psychophysical responses in retrobulbar neuritis. Ophthalmic Physiol Opt 4(1):101–105

    PubMed  CAS  Google Scholar 

  • Baier ML, Cutter GR, Rudick RA, Miller D, Cohen JA, Weinstock-Guttman B, Mass M, Balcer LJ (2005) Low-contrast letter acuity testing captures visual dysfunction in patients with multiple sclerosis. Neurology 64(6):992–995. doi:10.1212/01.WNL.0000154521.40686.63

    Article  PubMed  CAS  Google Scholar 

  • Bradley A, Zang L, Thibos LN (1992) Failures of isoluminance caused by ocular chromatic aberration. Appl Opt 31:3657–3667

    Article  PubMed  CAS  Google Scholar 

  • Callaway EM (2005) Structure and function of parallel pathways in the primate early visual system. J Physiol 566(Pt 1):13–19. doi:10.1113/jphysiol.2005.088047

    Article  PubMed  CAS  Google Scholar 

  • Cavanagh P, Tyler CW, Favreau OE (1984) Perceived velocity of moving chromatic gratings. J Opt Soc Am A 1(8):893–899

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Callaway EM (2003) Parallel colour-opponent pathways to primary visual cortex. Nature 426(6967):668–671. doi:10.1038/nature02167

    Article  PubMed  CAS  Google Scholar 

  • Cole GR, Hine T, McIlhagga W (1993) Detection mechanisms in L-, M-, and S-cone contrast space. J Opt Soc Am A 10(1):38–51

    Article  PubMed  CAS  Google Scholar 

  • Dacey DM (1993a) The mosaic of midget ganglion cells in the human retina. J Neurosci 13(12):5334–5355

    PubMed  CAS  Google Scholar 

  • Dacey DM (1993b) Morphology of a small-field bistratified ganglion cell type in the macaque and human retina. Vis Neurosci 10(6):1081–1098

    Article  PubMed  CAS  Google Scholar 

  • Dacey DM (2000) Parallel pathways for spectral coding in primate retina. Annu Rev Neurosci 23:743–775. doi:10.1146/annurev.neuro.23.1.743

    Article  PubMed  CAS  Google Scholar 

  • Dacey DM (2004) Origins of perception: retinal ganglion cell diversity and the creation of parallel visual pathways. In: Gazzaniga MS (ed) The cognitive neurosciences, III. MIT, Cambridge, pp 281–301

    Google Scholar 

  • Dacey DM, Packer OS (2003) Colour coding in the primate retina: diverse cell types and cone-specific circuitry. Curr Opin Neurobiol 13(4):421–427

    Article  PubMed  CAS  Google Scholar 

  • Dain SJ, Rammohan KW, Benes SC, King-Smith PE (1990) Chromatic, spatial, and temporal losses of sensitivity in multiple sclerosis. Invest Ophthalmol Vis Sci 31(3):548–558

    PubMed  CAS  Google Scholar 

  • Derrington AM, Krauskopf J, Lennie P (1984) Chromatic mechanisms in lateral geniculate nucleus of macaque. J Physiol 357:241–265

    Google Scholar 

  • Derrington AM, Lennie P (1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol 357:219–240

    PubMed  CAS  Google Scholar 

  • Eskew RT, McLellan JS, Giulianini F (1999) Chromatic detection and discrimination. In: Gegenfurtner KR, Sharpe LT (eds) Color vision: from molecular genetics to perception. Cambridge University Press, Cambridge, pp 345–368

    Google Scholar 

  • Eskin TA, Merigan WH (1986) Selective acrylamide-induced degeneration of color opponent ganglion cells in macaques. Brain Res 378(2):379–384

    Article  PubMed  CAS  Google Scholar 

  • Eskin TA, Lapham LW, Maurissen JP, Merigan WH (1985) Acrylamide effects on the macaque visual system. II. Retinogeniculate morphology. Invest Ophthalmol Vis Sci 26(3):317–329

    Google Scholar 

  • Fallowfield L, Krauskopf J (1984) Selective loss of chromatic sensitivity in demyelinating disease. Invest Ophthalmol Vis Sci 25(6):771–773

    PubMed  CAS  Google Scholar 

  • Ferrera VP, Nealey TA, Maunsell JH (1994) Responses in macaque visual area V4 following inactivation of the parvocellular and magnocellular LGN pathways. J Neurosci 14(4):2080–2088

    PubMed  CAS  Google Scholar 

  • Flanagan P, Markulev C (2005) Spatio-temporal selectivity of loss of colour and luminance contrast sensitivity with multiple sclerosis and optic neuritis. Ophthalmic Physiol Opt 25(1):57–65. doi:10.1111/j.1475-1313.2004.00252.x

    Article  PubMed  Google Scholar 

  • Flanagan P, Zele AJ (2004) Chromatic and luminance losses with multiple sclerosis and optic neuritis measured using dynamic random luminance contrast noise. Ophthalmic Physiol Opt 24(3):225–233. doi:10.1111/j.1475-1313.2004.00191.x

    Article  PubMed  Google Scholar 

  • Grigsby SS, Vingrys AJ, Benes SC, King-Smith PE (1991) Correlation of chromatic, spatial, and temporal sensitivity in optic nerve disease. Invest Ophthalmol Vis Sci 32(13):3252–3262

    PubMed  CAS  Google Scholar 

  • Hess RF, Plant GT (1986a) Optic neuritis. Cambridge University Press, Cambridge

    Google Scholar 

  • Hess RF, Plant GT (1986b) Optic neuritis. Ann Neurol 22(5):152–191

    Google Scholar 

  • Kaplan E, Shapley RM (1982) X and Y cells in the lateral geniculate nucleus of macaque monkeys. J Physiol 330:125–143

    PubMed  CAS  Google Scholar 

  • Kelly DH (1983) Spatiotemporal variation of chromatic and achromatic contrast thresholds. J Opt Soc Am 73(6):742–750

    Article  PubMed  CAS  Google Scholar 

  • Lankheet MJ, Lennie P, Krauskopf J (1998) Distinctive characteristics of subclasses of red-green P-cells in LGN of macaque. Vis Neurosci 15(1):37–46

    PubMed  CAS  Google Scholar 

  • Lee BB (2011) Visual pathways and psychophysical channels in the primate. J Physiol 589(Pt 1):41–47. doi:10.1113/jphysiol.2010.192658

    Article  PubMed  CAS  Google Scholar 

  • Lee BB, Sun H (2009) The chromatic input to cells of the magnocellular pathway of primates. J Vis 9(2):15.1–18

    Google Scholar 

  • Lee BB, Martin PR, Valberg A (1988) The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina. J Physiol 404:323–347

    PubMed  CAS  Google Scholar 

  • Lee BB, Pokorny J, Smith VC, Martin PR, Valberg A (1990) Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. J Opt Soc Am A 7(12):2223–2236

    Article  PubMed  CAS  Google Scholar 

  • Lennie P (1993) Roles of M and P pathways. In: Shapely R, Lam D (eds) Contrast sensitivity. MIT Press, Cambridge, pp 201–213

    Google Scholar 

  • Lennie P (1998) Single units and visual cortical organization. Perception 27(8):889–935

    Article  PubMed  CAS  Google Scholar 

  • Lennie P, Movshon JA (2005) Coding of color and form in the geniculostriate visual pathway (invited review). J Opt Soc Am A Opt Image Sci Vis 22(10):2013–2033

    Article  PubMed  Google Scholar 

  • Levitt JB, Schumer RA, Sherman SM, Spear PD, Movshon JA (2001) Visual response properties of neurons in the LGN of normally reared and visually deprived macaque monkeys. J Neurophysiol 85(5):2111–2129

    PubMed  CAS  Google Scholar 

  • Martin PR, White AJ, Goodchild AK, Wilder HD, Sefton AE (1997) Evidence that blue-on cells are part of the third geniculocortical pathway in primates. Eur J Neurosci 9(7):1536–1541

    Article  PubMed  CAS  Google Scholar 

  • Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4(9):877–886. doi:10.1038/nn0901-877

    Article  PubMed  CAS  Google Scholar 

  • Maunsell JH, Nealey TA, DePriest DD (1990) Magnocellular and parvocellular contributions to responses in the middle temporal visual area (MT) of the macaque monkey. J Neurosci 10(10):3323–3334

    PubMed  CAS  Google Scholar 

  • Merigan WH (1989) Chromatic and achromatic vision of macaques: role of the P pathway. J Neurosci 9(3):776–783

    PubMed  CAS  Google Scholar 

  • Merigan WH, Eskin TA (1986) Spatio-temporal vision of macaques with severe loss of P beta retinal ganglion cells. Vis Res 26(11):1751–1761

    Article  PubMed  CAS  Google Scholar 

  • Merigan WH, Maunsell JH (1990) Macaque vision after magnocellular lateral geniculate lesions. Vis Neurosci 5(4):347–352

    Article  PubMed  CAS  Google Scholar 

  • Merigan WH, Maunsell JH (1993) How parallel are the primate visual pathways? Annu Rev Neurosci 16:369–402. doi:10.1146/annurev.ne.16.030193.002101

    Article  PubMed  CAS  Google Scholar 

  • Merigan WH, Barkdoll E, Maurissen JP, Eskin TA, Lapham LW (1985) Acrylamide effects on the macaque visual system. I. Psychophysics and electrophysiology. Invest Ophthalmol Vis Sci 26(3):309–316

    Google Scholar 

  • Merigan WH, Katz LM, Maunsell JH (1991) The effects of parvocellular lateral geniculate lesions on the acuity and contrast sensitivity of macaque monkeys. J Neurosci 11(4):994–1001

    PubMed  CAS  Google Scholar 

  • Mullen KT (1985) The contrast sensitivity of human colour vision to red-green and blue-yellow chromatic gratings. J Physiol 359:381–400

    PubMed  CAS  Google Scholar 

  • Mullen KT, Plant GT (1986) Colour and luminance vision in human optic neuritis. Brain 109(Pt 1):1–13

    Article  PubMed  Google Scholar 

  • Mullen KT, Plant GT (1987) Anomalies in the appearance of colours and of hue discrimination in optic neuritis. Clin Vis Sci 1:287–302

    Google Scholar 

  • Rodieck RW, Watanabe M (1993) Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. J Comp Neurol 338(2):289–303. doi:10.1002/cne.903380211

    Article  PubMed  CAS  Google Scholar 

  • Russell MH, Murray IJ, Metcalfe RA, Kulikowski JJ (1991) The visual defect in multiple sclerosis and optic neuritis. A combined psychophysical and electrophysiological investigation. Brain 114(Pt 6):2419–2435

    Google Scholar 

  • Sankeralli MJ, Mullen KT (1996) Estimation of the L-, M- and S-cone weights of the post-receptoral detection mechanisms. J Optic Soc Am A 13:906–915

    Article  Google Scholar 

  • Schiller PH, Logothetis NK (1990) The color-opponent and broad-band channels of the primate visual system. Trends Neurosci 13(10):392–398

    Article  PubMed  CAS  Google Scholar 

  • Schneck ME, Haegerstrom-Portnoy G (1997) Color vision defect type and spatial vision in the optic neuritis treatment trial. Invest Ophthalmol Vis Sci 38(11):2278–2289

    PubMed  CAS  Google Scholar 

  • Sclar G, Maunsell JH, Lennie P (1990) Coding of image contrast in central visual pathways of the macaque monkey. Vis Res 30(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Smith VC, Pokorny J (1975) Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vis Res 15(2):161–171

    Article  PubMed  CAS  Google Scholar 

  • Solomon SG, White AJ, Martin PR (1999) Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus. J Physiol 517(Pt 3):907–917

    Article  PubMed  CAS  Google Scholar 

  • Tansey EM, Pessoa VF, Fleming S, Landon DN, Ikeda H (1985) Pattern and extent of demyelination in the optic nerves of mice infected with Semliki Forest virus and the possibility of axonal sprouting. Brain 108(Pt 1):29–41

    Article  PubMed  Google Scholar 

  • Travis D, Thompson P (1989) Spatiotemporal contrast sensitivity and colour vision in multiple sclerosis. Brain 112(Pt 2):283–303

    Article  PubMed  Google Scholar 

  • Trobe JD, Beck RW, Moke PS, Cleary PA (1996) Contrast sensitivity and other vision tests in the optic neuritis treatment trial. Am J Ophthalmol 121(5):547–553

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We extend our sincere gratitude to all of the subjects with ON who donated their time to help us collect data and especially to the subjects NK and GF who spent considerable time and effort to come to the laboratory on many occasions. We also thank all the control subjects for their time. We are grateful for the kind cooperation of the referring physicians (Drs. Jack Antel, Yves LaPierre, Amit Bar-Or, William Barkas and Francine Wein) and the help of Stanley Hum and Pamela Ng with patient records. This research was supported by a Canadian Institutes of Health Research (CIHR) grant MOP-10819 to KTM.

Author information

Authors and Affiliations

  1. McGill Vision Research, Department of Ophthalmology H4.14, McGill University, 687 Pine Ave West, Montreal, QC, H3A 1A1, Canada

    Amal M. Al-Hashmi, Daniel J. Kramer & Kathy T. Mullen

Authors
  1. Amal M. Al-Hashmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel J. Kramer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kathy T. Mullen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kathy T. Mullen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Al-Hashmi, A.M., Kramer, D.J. & Mullen, K.T. Human vision with a lesion of the parvocellular pathway: an optic neuritis model for selective contrast sensitivity deficits with severe loss of midget ganglion cell function. Exp Brain Res 215, 293–305 (2011). https://doi.org/10.1007/s00221-011-2896-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-011-2896-4

Keywords

Search

Navigation