Skip to main content

Advertisement

Log in

Dendritic Cell Factor 1-Knockout Results in Visual Deficit Through the GABA System in Mouse Primary Visual Cortex

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

The visual system plays an important role in our daily life. In this study, we found that loss of dendritic cell factor 1 (DCF1) in the primary visual cortex (V1) caused a sight deficit in mice and induced an abnormal increase in glutamic acid decarboxylase 67, an enzyme that catalyzes the decarboxylation of glutamate to gamma aminobutyric acid and CO2, particularly in layer 5. In vivo electrophysiological recordings confirmed a decrease in delta, theta, and beta oscillation power in DCF1-knockout mice. This study presents a previously unknown function of DCF1 in V1, suggests an unknown contact between DCF1 and GABA systems, and provides insight into the mechanism and treatment of visual deficits.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Sarihi A, Mirnajafi-Zadeh J, Jiang B, Sohya K, Safari MS, Arami MK, et al. Cell type-specific, presynaptic LTP of inhibitory synapses on fast-spiking GABAergic neurons in the mouse visual cortex. J Neurosci 2012, 32: 13189–13199.

    Article  PubMed  CAS  Google Scholar 

  2. Kirmse K, Kirischuk S. Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 2006, 26: 4216–4227.

    Article  PubMed  CAS  Google Scholar 

  3. Katzner S, Busse L, Carandini M. GABAA inhibition controls response gain in visual cortex. J Neurosci 2011, 31: 5931–5941.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Pinal CS, Tobin AJ. Uniqueness and redundancy in GABA production. Perspect Dev Neurobiol 1998, 5: 109–118.

    PubMed  CAS  Google Scholar 

  5. Soghomonian JJ, Martin DL. Two isoforms of glutamate decarboxylase: why? Trends Pharmacol Sci 1998, 19: 500–505.

    Article  PubMed  CAS  Google Scholar 

  6. Asada H, Kawamura Y, Maruyama K, Kume H, Ding RG, Kanbara N, et al. Cleft palate and decreased brain gamma-aminobutyric acid in mice lacking the 67-kDa isoform of glutamic acid decarboxylase. Proc Natl Acad Sci U S A 1997, 94: 6496–6499.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. Liu Q, Feng R, Chen Y, Luo G, Yan H, Chen L, et al. Dcf1 Triggers dendritic spine formation and facilitates memory acquisition. Mol Neurobiol 2017. doi: https://doi.org/10.1007/s12035-016-0349-6.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Wen T, Gu P, Chen F. Discovery of two novel functional genes from differentiation of neural stem cells in the striatum of the fetal rat. Neurosci Lett 2002, 329: 101–105.

    Article  PubMed  CAS  Google Scholar 

  9. Li X, Feng R, Huang C, Wang H, Wang J, Zhang Z, et al. MicroRNA-351 regulates TMEM 59 (DCF1) expression and mediates neural stem cell morphogenesis. RNA Biol 2012, 9: 292–301.

    Article  PubMed  CAS  Google Scholar 

  10. Wang L, Wang J, Wu Y, Wu J, Pang S, Pan R, et al. A novel function of dcf1 during the differentiation of neural stem cells in vitro. Cell Mol Neurobiol 2008, 28: 887–894.

    Article  PubMed  Google Scholar 

  11. Thaung C, Arnold K, Jackson IJ, Coffey PJ. Presence of visual head tracking differentiates normal sighted from retinal degenerate mice. Neurosci Lett 2002, 325: 21–24

    Article  PubMed  CAS  Google Scholar 

  12. Leitner FC, Melzer S, Lutcke H, Pinna R, Seeburg PH, Helmchen F, et al. Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nat Neurosci 2016, 19: 935–944.

    Article  PubMed  CAS  Google Scholar 

  13. Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. Chronux: A platform for analyzing neural signals. J Neurosci Methods 2010, 192: 146–151.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Watanabe M. Glutamate signaling and neural plasticity. No To Hattatsu 2013, 45: 267–274.

    PubMed  Google Scholar 

  15. Irwin RP, Allen CN. GABAergic signaling induces divergent neuronal Ca2+ responses in the suprachiasmatic nucleus network. Eur J Neurosci 2009, 30: 1462–1475.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Jiang L, Kundu S, Lederman JD, Lopez-Hernandez GY, Ballinger EC, Wang S, et al. Cholinergic signaling controls conditioned fear behaviors and enhances plasticity of cortical-amygdala circuits. Neuron 2016, 90: 1057–1070.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Chattopadhyaya B, Di Cristo G, Wu CZ, Knott G, Kuhlman S, Fu Y, et al. GAD67-mediated GABA synthesis and signaling regulate inhibitory synaptic innervation in the visual cortex. Neuron 2007, 54: 889–903.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Pothuizen HH, Davies M, Albasser MM, Aggleton JP, Vann SD. Granular and dysgranular retrosplenial cortices provide qualitatively different contributions to spatial working memory: evidence from immediate-early gene imaging in rats. Euro J Neurosci 2009 30: 877–888.

    Article  Google Scholar 

  19. Yamada Y, Hada Y, Imamura K, Mataga N, Watanabe Y, Yamamoto M. Differential expression of immediate-early genes, c-fos and zif268, in the visual cortex of young rats: Effects of a noradrenergic neurotoxin on their expression. Neuroscience 1999, 92: 473–484.

    Article  PubMed  CAS  Google Scholar 

  20. Zhu XO, McCabe BJ, Aggleton JP, Brown MW. Mapping visual recognition memory through expression of the immediate early gene c-fos. Neuroreport 1996, 7: 1871–1875.

    Article  PubMed  CAS  Google Scholar 

  21. Heeger DJ. Normalization of cell responses in cat striate cortex. Vis Neurosci 1992, 9:181–197.

    Article  PubMed  CAS  Google Scholar 

  22. Busse L, Wade A, Carandini M. Representation of concurrent stimuli by population activity in visual cortex. Neuron 2009, 64: 931–942

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Bonds AB. Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis Neurosci 1989, 2: 41–55.

    Article  PubMed  CAS  Google Scholar 

  24. Carandini M HD. Summation and division by neurons in primate visual cortex. Science 1994, 264: 1333–1336.

    Article  PubMed  CAS  Google Scholar 

  25. Carandini M HD, Movshon JA. Linearity and normalization in simple cells of the macaque primary visual cortex. J Neurosci 1997, 17: 8621–8644.

    Article  PubMed  CAS  Google Scholar 

  26. Morrone MC, Burr DC, Maffei L. Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc Lond B Biol Sci 1982, 216: 335–354.

    Article  PubMed  CAS  Google Scholar 

  27. Somers DC, Todorov EV, Siapas AG, Toth LJ, Kim DS, Sur M. A local circuit approach to understanding integration of long-range inputs in primary visual cortex. Cereb Cortex 1998, 8: 204–217.

    Article  PubMed  CAS  Google Scholar 

  28. Sohal VS. Insights into cortical oscillations arising from optogenetic studies. Biol Psychiatry 2012, 71: 1039–1045.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Biau E, Torralba M, Fuentemilla L, de Diego Balaguer R, Soto-Faraco S. Speaker’s hand gestures modulate speech perception through phase resetting of ongoing neural oscillations. Cortex 2015, 68: 76–85.

    Article  PubMed  Google Scholar 

  30. Rainer G, Lee H, Simpson GV, Logothetis NK. Working-memory related theta (4–7 Hz) frequency oscillations observed in monkey extrastriate visual cortex. Neurocomputing 2004, 58-60: 965–969.

    Article  Google Scholar 

  31. Schubert JT, Buchholz VN, Focker J, Engel AK, Roder B, Heed T. Oscillatory activity reflects differential use of spatial reference frames by sighted and blind individuals in tactile attention. Neuroimage 2015, 117: 417–428.

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (81271253 and 81471162), the Science and Technology Commission of Shanghai Municipality, China (14JC1402400), and the Key Innovation Project of Shanghai Municipal Education Commission, China (14ZZ090).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tieqiao Wen.

Ethics declarations

Conflict of interest

All authors claim that there are no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Shi, J., Li, Q. & Wen, T. Dendritic Cell Factor 1-Knockout Results in Visual Deficit Through the GABA System in Mouse Primary Visual Cortex. Neurosci. Bull. 34, 465–475 (2018). https://doi.org/10.1007/s12264-018-0211-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-018-0211-0

Keywords

Navigation