Skip to main content

Advertisement

Log in

Effects of autonomic denervations on the rhythms in axial length and choroidal thickness in chicks

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

In chicks, axial length and choroidal thickness undergo circadian oscillations. The choroid is innervated by both branches of the autonomic nervous system, but their contribution(s) to these rhythms is unknown. We used two combination lesions to test this. For parasympathectomy, nerve VII was sectioned presynaptic to the pterygopalatine ganglia, and the ciliary post-ganglionics were cut (double lesion; n = 8). Triple lesions excised the sympathetic superior cervical ganglion as well (n = 8). Sham surgery was done in controls (n = 7). 8–14 days later, axial dimensions were measured with ultrasonography at 4-h intervals over 24 h. Rhythm parameters were assessed using a “best fit” function, and growth rates measured. Both types of lesions resulted in ultradian (> 1 cycle/24 h) rhythms in choroidal thickness and axial length, and increased vitreous chamber growth (Exp-fellow: double: 69 µm; triple: 104 µm; p < 0.05). For double lesions, the frequency was 1.5 cycles/day for both rhythms; for triples the choroidal rhythm was 1.5 cycles/day, and the axial was 3 cycles/day. For double lesions, the amplitudes of both rhythms were larger than those of sham surgery controls (axial: 107 vs 54 µm; choroid: 124 vs 29 µm, p < 0.05). These findings provide evidence for the involvement of abnormal ocular rhythms in the growth stimulation underlying myopia development.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Notes

  1. We do not know how long the cell bodies in the pterygopalatine ganglia remain intact following the pre-synaptic lesion, but it is generally accepted that a pre-synaptic lesion will substantially reduce transmission via the post-synaptic pathway.

Abbreviations

ARVO:

Association for Research in Vision and Ophthalmology

CG:

Ciliary ganglion

CGX:

Ciliary ganglion lesion

N VII:

Cranial nerve VII

PPG:

Pterygopalatine ganglia

PPGX:

Pterygopalatine ganglion pre-synaptic (NVII) lesion

RPE:

Retinal pigment epithelium

References

  • Blessing W, Ootsuka Y (2016) Timing of activities of daily life is jaggy: how episodic ultradian changes in body and brain temperature are integrated into this process. Temperature 3:371–383

    Article  Google Scholar 

  • Bourguignon C, Storch KF (2017) Control of rest: activity by a dopaminergic ultradian oscillator and the circadian clock. Front Neurol 8:614

    Article  PubMed  PubMed Central  Google Scholar 

  • Buijs RM, Fleur SE, Wortel J, van Heyningen C, Zuiddam L, Mettenleiter TC, Kalsbeek A, Nagai K, Niijima A (2003) The suprachiasmatic nucleus balances sympathetic and parasympathetic output to peripheral organs through separate preautonomic neurons. J Comp Neurol 464:36–48

    Article  PubMed  Google Scholar 

  • Chakraborty R, Ostrin L, Nickla D, Iuvone P, Pardue M, Stone RA (2018) Circadian rhythms, refractive development, and myopia. Ophthalmic Physiol Opt 38:217–245

    Article  PubMed  PubMed Central  Google Scholar 

  • De Stefano M, Mugnaini E (1997) Fine structure of the choroidal coat of the avian eye: lymphatic vessels. Investig Ophthalmol Vis Sci 38:1241–1260

    Google Scholar 

  • Lauber JK, Boyd JE, Boyd TAS (1972) Sympathetic denervation effects of avian eye development and aqueous fluid dynamics. Proc Soc Exp Biol Med 140:351–356

    Article  CAS  PubMed  Google Scholar 

  • Lin T, Zhu X, Capehart C, Stone RA (1996) The ciliary ganglion and vitreous cavity shape. Curr Eye Res 15:453–460

    Article  CAS  PubMed  Google Scholar 

  • Marzani D, Wallman J (1997) Growth of the two layers of the chick sclera is modulated reciprocally by visual conditions. Investig Ophthalmol Vis Sci 38:1726–1739

    CAS  Google Scholar 

  • McDougal DH, Gamlin PD (2015) Autonomic control of the eye. Compr Physiol 5:439–473

    PubMed  PubMed Central  Google Scholar 

  • Meriney S, Pilar G (1987) Cholinergic innervation of the smooth muscle cells in the choroid coat of the chick eye and its development. J Neurosci 7:3827–3839

    Article  CAS  PubMed  Google Scholar 

  • Nickla D (2005) The phase relationships between the diurnal rhythm in axial length and choroidal thickness and the association with ocular growth rate in chicks. J Comp Physiol A 192:399–407

    Article  Google Scholar 

  • Nickla DL, Schroedl F (2012a) The effects of double parasympathectomy on the diurnal rhythms in choroidal thickness and axial length in chicks. ARVO E-Abstract #3433

  • Nickla DL, Schroedl F (2012b) Parasympathetic influences on emmetropization in chicks: evidence for different mechanisms in form deprivation vs negative lens-induced myopia. Exp Eye Res 102:93–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nickla DL, Wallman J (2010) The multifunctional choroid. Prog Retin Eye Res 29:144–168

    Article  PubMed  Google Scholar 

  • Nickla DL, Wildsoet C, Wallman J (1998) Visual influences on diurnal rhythms in ocular length and choroidal thickness in chick eyes. Exp Eye Res 66:163–181

    Article  CAS  PubMed  Google Scholar 

  • Nickla DL, Rada JA, Wallman J (1999) Isolated chick sclera shows a circadian rhythm in proteoglycan synthesis perhaps associated with the rhythm in ocular elongation. J Comp Physiol [A] 185:81–90

    Article  CAS  Google Scholar 

  • Ohngemach S, Feldkaemper MP, Schaeffel F (2001) Pineal control of the dopamine D2-receptor gene and dopamine release in the retina of the chicken and their possible relation to growth rhythms of the eye. J Pineal Res 31:145–154

    Article  CAS  PubMed  Google Scholar 

  • Papastergiou GI, Schmid G, Riva CE, Mendel MJ, Stone RA, Laties AM (1998) Ocular axial length and choroidal thickness in newly hatched chicks and one-year-old chickens fluctuate in a diurnal pattern that is influenced by visual experience and intraocular pressure changes. Exp Eye Res 66:195–205

    Article  CAS  PubMed  Google Scholar 

  • Rada JA, Thoft RA, Hassell JR (1990) Extracellular matrix changes in the sclera of chickens with experimental myopia. Investig Ophthal (ARVO Suppl) 31:253

    Google Scholar 

  • Rada JA, Thoft RA, Hassell JR (1991) Increased aggrecan (cartilage proteoglycan) production in the sclera of myopic chicks. Dev Biol 147:303–312

    Article  CAS  PubMed  Google Scholar 

  • Rada JA, McFarland AL, Cornuet PK, Hassell JR (1992) Proteoglycan synthesis by scleral chondrocytes is modulated by a vision dependent mechanism. Curr Eye Res 11:767–782

    Article  CAS  PubMed  Google Scholar 

  • Reiner A, Karten HJ, Gamlin PDR, Erichsen J (1983) Functional subdivisions and circuitry of the avian nucleus of Edinger–Westphal. TINS 6:140–145

    Google Scholar 

  • Rucker F, Troilo D, Zhu X, Bitzer M, Schaeffel F, Wallman J (2009) Interocular lens interactions in lens compensation: yoking and anti-yoking. Investig Ophthalmol Vis Sci 50:3931

    Article  Google Scholar 

  • Schmid K, Wildsoet CF (1996) Effects of the compensatory responses to positive and negative lenses of intermittent lens wear and ciliary nerve section in chicks. Vis Res 36:1023–1036

    Article  CAS  PubMed  Google Scholar 

  • Schmid GF, Papastergiou GI, Lin T, Riva CE, Laties AM, Stone RA (1999) Autonomic denervations influence ocular dimensions and intraocular pressure in chicks. Exp Eye Res 68:573–581

    Article  CAS  PubMed  Google Scholar 

  • Schroedl F, Tines R, Brehmer A, Neuhuber W (2001) Intrinsic choroidal neurons in the duck eye receive sympathetic input: anatomical evidence for adrenergic modulation of nitrergic functions in the choroid. Cell Tissue Res 304:175–184

    Article  Google Scholar 

  • Smith EL, Hung LF, Kee CS, Qiao Y (2002) Effects of brief periods of unrestricted vision on the development of form deprivation myopia in monkeys. Investig Ophthalmol Vis Sci 43:291–299

    Google Scholar 

  • Stone RA, Wei W, Sarfare S, Pan W, Engelhart KC, Khurana T, McGuire MG, Iuvone PM, Nickla D (2018) Diurnal cycling of clock and melanopsin genes in chick choroid. ARVO E-Abstract #5048

  • Stubinger K, Brehmer A, Neuhuber WL, Reitsamer H, Nickla DL, Schroedl F (2010) Intrinsic choroidal neurons in the chicken eye: chemical coding and synaptic input. Histochem Cell Biol 134:145–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vujovic N, Davidson AJ, Menaker M (2008) Sympathetic input modulates, but does not determine, phase of peripheral circadian oscillators. Am J Physiol Regul Integr Comp Physiol 295:355–360

    Article  CAS  Google Scholar 

  • Wallman J, Winawer J (2004) Homeostasis of eye growth and the question of myopia. Neuron 43:447–468

    Article  CAS  PubMed  Google Scholar 

  • Wallman J, Wildsoet C, Xu A, Gottlieb M, Nickla D, Marran L, Krebs W, Christensen A (1995) Moving the retina: choroidal modulation of refractive state. Vis Res 35:37–50

    Article  CAS  PubMed  Google Scholar 

  • Weiss S, Schaeffel F (1993) Diurnal growth rhythms in the chicken eye: relation to myopia development and retinal dopamine levels. J Comp Physiol A 172:263–270

    Article  CAS  PubMed  Google Scholar 

  • Wildsoet C, Wallman J (1995) Choroidal and scleral mechanisms of compensation for spectacle lenses in chicks. Vis Res 35:1175–1194

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was funded by the National Eye Institute NIH-NEI-013636 and NIH-NEI-025307. The authors thank Kristen Totonelly and Jonathan Elin-Calcador for collecting some of the data. Care and use of animals conformed to the ARVO Resolution for the Care and Use of Animals in Research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Debora L. Nickla.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nickla, D.L., Schroedl, F. Effects of autonomic denervations on the rhythms in axial length and choroidal thickness in chicks. J Comp Physiol A 205, 139–149 (2019). https://doi.org/10.1007/s00359-018-01310-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-018-01310-4

Keywords

Navigation