Short-Term Visual Experience Leads to Potentiation of Spontaneous Activity in Mouse Superior Colliculus

Neuroscience Bulletin (2021)Cite this article

Abstract

Spontaneous activity in the brain maintains an internal structured pattern that reflects the external environment, which is essential for processing information and developing perception and cognition. An essential prerequisite of spontaneous activity for perception is the ability to reverberate external information, such as by potentiation. Yet its role in the processing of potentiation in mouse superior colliculus (SC) neurons is less studied. Here, we used electrophysiological recording, optogenetics, and drug infusion methods to investigate the mechanism of potentiation in SC neurons. We found that visual experience potentiated SC neurons several minutes later in different developmental stages, and the similarity between spontaneous and visually-evoked activity increased with age. Before eye-opening, activation of retinal ganglion cells that expressed ChR2 also induced the potentiation of spontaneous activity in the mouse SC. Potentiation was dependent on stimulus number and showed feature selectivity for direction and orientation. Optogenetic activation of parvalbumin neurons in the SC attenuated the potentiation induced by visual experience. Furthermore, potentiation in SC neurons was blocked by inhibiting the glutamate transporter GLT1. These results indicated that the potentiation induced by a visual stimulus might play a key role in shaping the internal representation of the environment, and serves as a carrier for short-term memory consolidation.

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

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

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

References

  1. 1.

    Iemi L, Chaumon M, Crouzet SM, Busch NA. Spontaneous neural oscillations bias perception by modulating baseline excitability. J Neurosci 2017, 37: 807–819

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  2. 2.

    Berkes P, Orban G, Lengyel M, Fiser J. Spontaneous cortical activity reveals hallmarks of an optimal internal model of the environment. Science 2011, 331: 83–87

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  3. 3.

    Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A. Spontaneously emerging cortical representations of visual attributes. Nature 2003, 425: 954–956

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Fu YX, Djupsund K, Gao H, Hayden B, Shen K, Dan Y. Temporal specificity in the cortical plasticity of visual space representation. Science 2002, 296: 1999–2003

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Marques HG, Bharadwaj A, Iida F. From spontaneous motor activity to coordinated behaviour: a developmental model. PLoS Comput Biol 2014, 10: e1003653

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  6. 6.

    Wang X-j. Probabilistic decision making by slow reverberation in cortical circuits. Neuron 2002, 36: 955–968

    CAS  PubMed  Article  Google Scholar 

  7. 7.

    Mohajerani MH, Chan AW, Mohsenvand M, LeDue J, Liu R, McVea DA. Spontaneous cortical activity alternates between motifs defined by regional axonal projections. Nat Neurosci 2013, 16: 1426–1435

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Luczak A, Bartho P, Harris KD. Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 2009, 62: 413–425

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Han F, Caporale N, Dan Y. Reverberation of recent visual experience in spontaneous cortical waves. Neuron 2008, 60: 321–327

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Ackman JB, Crair MC. Role of emergent neural activity in visual map development. Curr Opin Neurobiol 2014, 24: 166–175

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  11. 11.

    Chiu C, Weliky M. Spontaneous activity in developing ferret visual cortex in vivo. J Neurosci 2001, 15: 8906–8914

    Article  Google Scholar 

  12. 12.

    Bonetti C, Surace EM. Mouse embryonic retina delivers information controlling cortical neurogenesis. PLoS One 2010, 5: e15211

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  13. 13.

    Hanson MG, Landmesser LT. Normal patterns of spontaneous activity are required for correct motor axon guidance and the expression of specific guidance molecules. Neuron 2004, 43: 687–701

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  14. 14.

    Penn AA, Riquelme PA, Feller MB, Shatz CJ. Competition in retinogeniculate patterning driven by spontaneous activity. Science 1998, 279: 2108–2112

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Kirkby LA, Sack GS, Firl A, Feller MB. A role for correlated spontaneous activity in the assembly of neural circuits. Neuron 2013, 80: 1129–1144

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. 16.

    Blankenship AG, Feller MB. Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nat Rev Neurosci 2010, 11: 18–29

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Xu HP, Furman M, Mineur YS, Chen H, King SL, Zenisek D, et al. An instructive role for patterned spontaneous retinal activity in mouse visual map development. Neuron 2011, 70: 1115–1127

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18.

    Wang K, Jiang T, Yu C, Tian L, Li J, Liu Y, et al. Spontaneous activity associated with primary visual cortex: a resting-state FMRI study. Cereb Cortex 2008, 18: 697–704

    PubMed  Article  Google Scholar 

  19. 19.

    Bliss TV, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361: 31–39

    CAS  PubMed  Article  Google Scholar 

  20. 20.

    Bortolotto ZA, Fitzjohn SM, Collingridge GL. Roles of metabotropic glutamate receptors in LTP and LTD in the hippocampus. Curr Opin Neurobiol 1999, 9: 299–304

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  21. 21.

    Katagiri H, Tanaka K, Manabe T. Requirement of appropriate glutamate concentrations in the synaptic cleft for hippocampal LTP induction. Eur J Neurosci 2001, 14: 547–553

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  22. 22.

    Goubard V, Fino E, Venance L. Contribution of astrocytic glutamate and GABA uptake to corticostriatal information processing. J Physiol 2011, 589: 2301–2319

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Tian SW, Yu XD, Cen L, Xiao ZY. Glutamate transporter GLT1 inhibitor dihydrokainic acid impairs novel object recognition memory performance in mice. Physiol Behav 2019, 199: 28–32

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  24. 24.

    Tzingounis AV, Wadiche JI. Glutamate transporters: confining runaway excitation by shaping synaptic transmission. Nat Rev Neurosci 2007, 8: 935–947

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  25. 25.

    Jensen AA, Fahlke C, Bjorn-Yoshimoto WE, Bunch L. Excitatory amino acid transporters: recent insights into molecular mechanisms, novel modes of modulation and new therapeutic possibilities. Curr Opin Pharmacol 2015, 20: 116–123

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  26. 26.

    He K, Huertas M, Hong SZ, Tie X, Hell JW, Shouval H, et al. Distinct eligibility traces for LTP and LTD in cortical synapses. Neuron 2015, 88: 528–538

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  27. 27.

    Pita-Almenar JD, Collado MS, Colbert CM, Eskin A. Different mechanisms exist for the plasticity of glutamate reuptake during early long-term potentiation (LTP) and late LTP. J Neurosci 2006, 26: 10461–10471

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. 28.

    Pita-Almenar JD, Zou S, Colbert CM, Eskin A. Relationship between increase in astrocytic GLT-1 glutamate transport and late-LTP. Learn Mem 2012, 19: 615–626

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. 29.

    Tsvetkov E, Shin R-M, Bolshakov VY. Glutamate uptake determines pathway specificity of long-term potentiation in the neural circuitry of fear conditioning. Neuron 2004, 41: 139–151

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  30. 30.

    Ito S, Feldheim DA. The Mouse superior colliculus: an emerging model for studying circuit formation and function. Front Neural Circuits 2018, 12: 10

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  31. 31.

    Ellis EM, Gauvain G, Sivyer B, Murphy GJ. Shared and distinct retinal input to the mouse superior colliculus and dorsal lateral geniculate nucleus. J Neurophysiol 2016, 116: 602–610

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Wang Q, Burkhalter A. Stream-related preferences of inputs to the superior colliculus from areas of dorsal and ventral streams of mouse visual cortex. J Neurosci 2013, 33: 1696–1705

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. 33.

    Madisen L, Mao T, Koch H, Zhuo JM, Berenyi A, Fujisawa S, et al. A toolbox of cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nat Neurosci 2012, 15: 793–802

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34.

    Leng T, Gao X, Dilger JP, Lin J. Neuroprotective effect of lidocaine: is there clinical potential? Int J Physiol Pathophysiol Pharmacol 2016, 8: 9–13

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Kalso E. Sodium channel blockers in neuropathic pain. Curr Pharm Des 2005, 11: 3005–3011

    CAS  PubMed  Article  Google Scholar 

  36. 36.

    Seabrook TA, Burbridge TJ, Crair MC, Huberman AD. Architecture, function, and assembly of the mouse visual system. Annu Rev Neurosci 2017, 40: 499–538

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Wang L, Sarnaik R, Rangarajan K, Liu X, Cang J. Visual receptive field properties of neurons in the superficial superior colliculus of the mouse. J Neurosci 2010, 30: 16573–16584

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  38. 38.

    Niell CM, Stryker MP. Highly selective receptive fields in mouse visual cortex. J Neurosci 2008, 28: 7520–7536

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Ackman JB, Burbridge TJ, Crair MC. Retinal waves coordinate patterned activity throughout the developing visual system. Nature 2012, 490: 219–225

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. 40.

    Wong RO. Retinal waves and visual system development. Annu Rev Neurosci 1999, 22: 29–47

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Anand R. Chandrasekaran DTP, Ernesto Gonzalez,and Michael C. Crair. Evidence for an instructive role of retinal activity in retinotopic map refinement in the superior colliculus of the mouse. J Neurosci 2005, 25: 6929–6938.

    Article  CAS  Google Scholar 

  42. 42.

    Thyagarajan S, van Wyk M, Lehmann K, Lowel S, Feng G, Wassle H. Visual function in mice with photoreceptor degeneration and transgenic expression of channelrhodopsin 2 in ganglion cells. J Neurosci 2010, 30: 8745–8758

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  43. 43.

    Shi X, Barchini J, Ledesma HA, Koren D, Jin Y, Liu X, et al. Retinal origin of direction selectivity in the superior colliculus. Nat Neurosci 2017, 20: 550–558

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. 44.

    Duan J, Fu H, Zhang J. Activation of parvalbumin-positive neurons in both retina and primary visual cortex improves the feature-selectivity of primary visual cortex neurons. Neurosci Bull 2017, 33: 255–263

    PubMed  PubMed Central  Article  Google Scholar 

  45. 45.

    Gray CM, Singer W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci U S A 1989, 86: 1698–1702

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  46. 46.

    De Valois RL, Yund EW, Hepler N. The orientation and direction selectivity of cells in macaque visual cortex. Vision Res 1982, 22: 531–544

    PubMed  Article  Google Scholar 

  47. 47.

    Kruskal JB, Wish M. Multidimensional scaling. SAGE Publications, London. 1978.

    Google Scholar 

  48. 48.

    Maesschalck RD, Jouan-Rimbaud D, Massart DL. The mahalanobis distance. chemometrics & intelligent laboratory systems 2000, 50: 1–18.

  49. 49.

    Deza MM, Deza E. Encyclopedia of distances. Reference Reviews 2009, 24: 1–583

    Google Scholar 

  50. 50.

    Lundstrom BN, Fairhall AL. Decoding stimulus variance from a distributional neural code of interspike intervals. J Neurosci 2006, 26: 9030–9037

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Gong LQ, He LJ, Dong ZY, Lu XH, Poo MM, Zhang XH. Postinduction requirement of NMDA receptor activation for late-phase long-term potentiation of developing retinotectal synapses in vivo. J Neurosci 2011, 31: 3328–3335

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52.

    Xu S, Jiang W, Poo MM, Dan Y. Activity recall in a visual cortical ensemble. Nat Neurosci 2012, 15(449–455): S441-442

    Google Scholar 

  53. 53.

    Lynch MA. Long-term potentiation and memory. Physiol Rev 2004, 84: 87–136

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. 54.

    Cooke SF, Bear MF. Visual experience induces long-term potentiation in the primary visual cortex. J Neurosci 2010, 30: 16304–16313

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  55. 55.

    Huberman AD, Feller MB, Chapman B. Mechanisms underlying development of visual maps and receptive fields. Annu Rev Neurosci 2008, 31: 479–509

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56.

    Espinosa JS, Stryker MP. Development and plasticity of the primary visual cortex. Neuron 2012, 75: 230–249

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57.

    Li N, Gu Y. The visual pathway for binocular integration. Neurosci Bull 2020, 36: 1089–1091.

    PubMed  Article  PubMed Central  Google Scholar 

  58. 58.

    White LE, Coppola DM, Fitzpatrick D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 2001, 411: 1049–1052

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  59. 59.

    Hensch TK. Critical period regulation. Annu Rev Neurosci 2004, 27: 549–579

    CAS  PubMed  Article  Google Scholar 

  60. 60.

    McLaughlin T, Torborg CL, Feller MB, O’Leary DDM. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development. Neuron 2003, 40: 1147–1160

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  61. 61.

    Hensch MFTK. Inhibitory threshold for critical-period activation in primary visual cortex. Nature 2000, 404: 4

    Google Scholar 

  62. 62.

    Hensch TK, Fagiolini M, Mataga N, Stryker MP, Baekkeskov S, Kash SF. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 1998, 282: 1504–1508

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  63. 63.

    Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, et al. Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 2010, 30: 361–371

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. 64.

    Maya-Vetencourt JF, Sale A, Viegi A, Baroncelli L, De Pasquale R, O’Leary OF, et al. The antidepressant fluoxetine restores plasticity in the adult visual cortex. Science 2008, 320: 385–388

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  65. 65.

    Sale A, Maya-Vetencourt JF, Medinin P, Cenni MC, Baroncelli L, De Pasquale R, et al. Environmental enrichment in adulthood promotes amblyopia recovery through a reduction of intracortical inhibition. Nat Neurosci 2007, 10: 679–681

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  66. 66.

    Gao WJ, Wormington AB, Newman DE, Pallas SL. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of calbindin- and parvalbumin-containing neurons. J Comp Neurol 2000, 422: 140–157

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  67. 67.

    Krishnan K, Wang B-S, Lu J, Wang L, Maffei A, Cang J, et al. MeCP2 regulates the timing of critical period plasticity that shapes functional connectivity in primary visual cortex. Proc Natl Acad Sci U S A 2015, 112: E4782–E4791

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  68. 68.

    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 2018, 34: 465–475

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  69. 69.

    Le Magueresse C, Monyer H. GABAergic interneurons shape the functional maturation of the cortex. Neuron 2013, 77: 388–405

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  70. 70.

    Gandhi NJ, Katnani HA. Motor functions of the superior colliculus. Annu Rev Neurosci 2011, 34: 205–231

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  71. 71.

    Alloway KD, Smith JB, Beauchemin KJ. Quantitative analysis of the bilateral brainstem projections from the whisker and forepaw regions in rat primary motor cortex. J Comp Neurol 2010, 518: 4546–4566

    PubMed  PubMed Central  Article  Google Scholar 

  72. 72.

    Killackey HP, RS. E. Trigeminal projections of the superior Colliculus of the rat. J Comp Neurol 1981, 201: 221–242.

  73. 73.

    Sparks DL, Lee C, Rohrer WH. Population coding of the direction, amplitude, and velocity of saccadic eye movements by neurons in the superior colliculus. Cold Spring Harb Symp Quant Biol 1990, 55: 805–811

    CAS  PubMed  Article  Google Scholar 

  74. 74.

    Liang F, Xiong XR, Zingg B, Ji XY, Zhang LI, Tao HW. Sensory cortical control of a visually induced arrest behavior via corticotectal projections. Neuron 2015, 86: 755–767

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  75. 75.

    Shang C, Liu Z, Chen Z, Shi Y, Wang Q, Liu S, et al. A parvalbumin-positive excitatory visual pathway to trigger fear responses in mice. Science 2015, 348: 1472–1477.

    CAS  PubMed  Article  Google Scholar 

  76. 76.

    Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain 2006, 129: 1659–1673

    CAS  PubMed  Article  Google Scholar 

  77. 77.

    Adams JP, Dudek SM. Late-phase long-term potentiation: getting to the nucleus. Nat Rev Neurosci 2005, 6: 737–743

    CAS  PubMed  Article  Google Scholar 

  78. 78.

    Yukio Seki PJF, Richard W. Keller, Bruce I. Tranmer, Harold K. Kimelberg. Inhibition of ischemia-induced glutamate release in rat striatum by dihydrokinate and an anion channel blocker. Stroke 1999, 30: 433–440.

  79. 79.

    Bechtholt-Gompf AJ, Walther HV, Adams MA, Carlezon WA Jr, Ongur D, Cohen BM. Blockade of astrocytic glutamate uptake in rats induces signs of anhedonia and impaired spatial memory. Neuropsychopharmacology 2010, 35: 2049–2059

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  80. 80.

    May PJ. The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 2006, 151: 321–378

    PubMed  Article  Google Scholar 

  81. 81.

    Feinberg EH, Meister M. Orientation columns in the mouse superior colliculus. Nature 2015, 519: 229–232

    CAS  PubMed  Article  Google Scholar 

  82. 82.

    Kerschensteiner D. Glutamatergic retinal waves. Front Neural Circuits 2016, 10: 38

    PubMed  PubMed Central  Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31771195, 81790640 and 82021002), a Shanghai Municipal Science and Technology Major Project (2018SHZDZX01) and ZJLab, Key Scientific Technological Innovation Research Project of the Ministry of Education, Sanming Project of Medicine in Shenzhen (SZSM202011015) and Shanghai Health and Family Planning Commission (20164Y0096, 20184Y0184).

Author information

Author notes

  1. Qingpeng Yu, Hang Fu and Gang Wang contributed equally to this work.

Affiliations

  1. Institutes of Brain Science, State Key Laboratory of Medical Neurobiology and Ministry of Education Frontiers Center for Brain Science, Department of Ophthalmology, Zhongshan Hospital, Fudan University, Shanghai, 200433, China

    Qingpeng Yu, Hang Fu, Jiayi Zhang & Biao Yan

  2. Center of Brain Sciences, Beijing Institute of Basic Medical Sciences, No. 27, Taiping Road, Haidian District, Beijing, 100850, China

    Gang Wang

Authors
  1. Qingpeng Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hang Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiayi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Biao Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jiayi Zhang or Biao Yan.

Ethics declarations

Conflict of interest

The 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 241 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yu, Q., Fu, H., Wang, G. et al. Short-Term Visual Experience Leads to Potentiation of Spontaneous Activity in Mouse Superior Colliculus. Neurosci. Bull. (2021). https://doi.org/10.1007/s12264-020-00622-3

Download citation

Keywords

  • Spontaneous activity
  • Visual experience
  • Potentiation
  • Superior colliculus
  • Feature selectivity
  • Glutamate homeostasis