GABAergic circuits control stimulus-instructed receptive field development in the optic tectum

Abstract

During the development of sensory systems, receptive fields are modified by stimuli in the environment. This is thought to rely on learning algorithms that are sensitive to correlations in spike timing between cells, but the manner in which developing circuits selectively exploit correlations that are related to sensory inputs is unknown. We recorded from neurons in the developing optic tectum of Xenopus laevis and found that repeated presentation of moving visual stimuli induced receptive field changes that reflected the properties of the stimuli and that this form of learning was disrupted when GABAergic transmission was blocked. Consistent with a role for spike timing–dependent mechanisms, GABA blockade altered spike-timing patterns in the tectum and increased correlations between cells that would affect plasticity at intratectal synapses. This is a previously unknown role for GABAergic signals in development and highlights the importance of regulating the statistics of spiking activity for learning.

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Figure 1: Examining stimulus-driven receptive field changes in tectal neurons.
Figure 2: Moving stimuli instruct asymmetric changes in tectal receptive fields.
Figure 3: Blocking GABAergic inputs eliminates instructive training effects on tectal receptive fields.
Figure 4: Effects of GABAA receptor blockade on baseline receptive field properties.
Figure 5: GABA blockade boosts temporal correlations between tectal neurons during training.
Figure 6: Receptive field changes are altered by manipulations of spike timing during training.
Figure 7: GABAergic circuits reduce spatiotemporal correlations in tectal receptive fields.
Figure 8: The timing of synaptic inputs underlies GABAergic control of tectal spiking.

References

  1. 1

    Goodman, C.S. & Shatz, C.J. Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72, 77–98 (1993).

    Article  Google Scholar 

  2. 2

    Katz, L.C. & Shatz, C.J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    CAS  Article  Google Scholar 

  3. 3

    Wiesel, T.N. & Hubel, D.H. Single-cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003–1017 (1963).

    CAS  Article  Google Scholar 

  4. 4

    Stryker, M.P. Evidence for a possible role for spontaneous electrical activity in the development of the mammalian visual cortex. in Problems and Concepts in Developmental Neurophysiology (eds. Kellaway, P. & Noebels, J.L.) 110–130 (John Hopkins University Press, Baltimore, 1989).

  5. 5

    Weliky, M. & Katz, L.C. Disruption of orientation tuning in visual cortex by artificially correlated neuronal activity. Nature 386, 680–685 (1997).

    CAS  Article  Google Scholar 

  6. 6

    Engert, F., Tao, H.W., Zhang, L.I. & Poo, M. Moving visual stimuli rapidly induce direction sensitivity of developing tectal neurons. Nature 419, 470–475 (2002).

    CAS  Article  Google Scholar 

  7. 7

    Li, Y., Van Hooser, S.D., Mazurek, M., White, L.E. & Fitzpatrick, D. Experience with moving visual stimuli drives the early development of cortical direction selectivity. Nature 456, 952–956 (2008).

    CAS  Article  Google Scholar 

  8. 8

    Meliza, C.D. & Dan, Y. Receptive-field modification in rat visual cortex induced by paired visual stimulation and single-cell spiking. Neuron 49, 183–189 (2006).

    CAS  Article  Google Scholar 

  9. 9

    Sengpiel, F., Stawinski, P. & Bonhoeffer, T. Influence of experience on orientation maps in cat visual cortex. Nat. Neurosci. 2, 727–732 (1999).

    CAS  Article  Google Scholar 

  10. 10

    Vislay-Meltzer, R.L., Kampff, A.R. & Engert, F. Spatiotemporal specificity of neuronal activity directs the modification of receptive fields in the developing retinotectal system. Neuron 50, 101–114 (2006).

    CAS  Article  Google Scholar 

  11. 11

    Mu, Y. & Poo, M. Spike timing–dependent LTP/LTD mediates visual experience–dependent plasticity in a developing retinotectal system. Neuron 50, 115–125 (2006).

    CAS  Article  Google Scholar 

  12. 12

    Schuett, S., Bonhoeffer, T. & Hübener, M. Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32, 325–337 (2001).

    CAS  Article  Google Scholar 

  13. 13

    Shon, A.P., Rao, R.P.N. & Sejnowski, T.J. Motion detection and prediction through spike-timing dependent plasticity. Network 15, 179–198 (2004).

    CAS  Article  Google Scholar 

  14. 14

    Wenisch, O.G., Noll, J. & Hemmen, J. Spontaneously emerging direction selectivity maps in visual cortex through STDP. Biol. Cybern. 93, 239–247 (2005).

    Article  Google Scholar 

  15. 15

    Weliky, M. Correlated neuronal activity and visual cortical development. Neuron 27, 427–430 (2000).

    CAS  Article  Google Scholar 

  16. 16

    Ramoa, A.S., Paradiso, M.A. & Freeman, R.D. Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity. Exp. Brain Res. 73, 285–296 (1988).

    CAS  Article  Google Scholar 

  17. 17

    Gabernet, L., Jadhav, S.P., Feldman, D.E., Carandini, M. & Scanziani, M. Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 48, 315–327 (2005).

    CAS  Article  Google Scholar 

  18. 18

    Pouille, F. & Scanziani, M. Enforcement of temporal fidelity in pyramidal cells by somatic feedforward inhibition. Science 293, 1159–1163 (2001).

    CAS  Article  Google Scholar 

  19. 19

    Wehr, M. & Zador, A.M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003).

    CAS  Article  Google Scholar 

  20. 20

    Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75–78 (1995).

    CAS  Article  Google Scholar 

  21. 21

    Akerman, C.J. & Cline, H.T. Depolarizing GABAergic conductances regulate the balance of excitation to inhibition in the developing retinotectal circuit in vivo. J. Neurosci. 26, 5117–5130 (2006).

    CAS  Article  Google Scholar 

  22. 22

    Dunning, D.D., Hoover, C.L., Soltesz, I., Smith, M.A. & O′Dowd, D.K. GABAA receptor–mediated miniature postsynaptic currents and alpha-subunit expression in developing cortical neurons. J. Neurophysiol. 82, 3286–3297 (1999).

    CAS  Article  Google Scholar 

  23. 23

    Hollrigel, G.S. & Soltesz, I. Slow kinetics of miniature IPSCs during early postnatal development in granule cells of the dentate gyrus. J. Neurosci. 17, 5119–5128 (1997).

    CAS  Article  Google Scholar 

  24. 24

    Liu, Y., Zhang, L.I. & Tao, H.W. Heterosynaptic scaling of developing GABAergic synapses: dependence on glutamatergic input and developmental stage. J. Neurosci. 27, 5301–5312 (2007).

    CAS  Article  Google Scholar 

  25. 25

    Tao, H.W. & Poo, M. Activity-dependent matching of excitatory and inhibitory inputs during refinement of visual receptive fields. Neuron 45, 829–836 (2005).

    CAS  Article  Google Scholar 

  26. 26

    Tyzio, R. et al. The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 19, 10372–10382 (1999).

    CAS  Article  Google Scholar 

  27. 27

    Luhmann, H.J. & Prince, D.A. Postnatal maturation of the GABAergic system in rat neocortex. J. Neurophysiol. 65, 247–263 (1991).

    CAS  Article  Google Scholar 

  28. 28

    Mueller, A.L., Taube, J.S. & Schwartzkroin, P.A. Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro. J. Neurosci. 4, 860–867 (1984).

    CAS  Article  Google Scholar 

  29. 29

    Zhang, L.I., Tao, H.W. & Poo, M. Visual input induces long-term potentiation of developing retinotectal synapses. Nat. Neurosci. 3, 708–715 (2000).

    CAS  Article  Google Scholar 

  30. 30

    Zhang, L.I., Tao, H.W., Holt, C.E., Harris, W.A. & Poo, M. A critical window for cooperation and competition among developing retinotectal synapses. Nature 395, 37–44 (1998).

    CAS  Article  Google Scholar 

  31. 31

    Gao, X.B. & Van Den Pol, A.N. GABA, not glutamate, a primary transmitter driving action potentials in developing hypothalamic neurons. J. Neurophysiol. 85, 425–434 (2001).

    CAS  Article  Google Scholar 

  32. 32

    Staley, K.J. & Mody, I. Shunting of excitatory input to dentate gyrus granule cells by a depolarizing GABAA receptor–mediated postsynaptic conductance. J. Neurophysiol. 68, 197–212 (1992).

    CAS  Article  Google Scholar 

  33. 33

    Ulrich, D. Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells. Eur. J. Neurosci. 18, 2159–2165 (2003).

    Article  Google Scholar 

  34. 34

    Gulledge, A.T. & Stuart, G.J. Excitatory actions of GABA in the cortex. Neuron 37, 299–309 (2003).

    CAS  Article  Google Scholar 

  35. 35

    Chen, G., Trombley, P.Q. & van den Pol, A.N. Excitatory actions of GABA in developing rat hypothalamic neurones. J. Physiol. (Lond.) 494, 451–464 (1996).

    CAS  Article  Google Scholar 

  36. 36

    Pratt, K.G., Dong, W. & Aizenman, C.D. Development and spike timing–dependent plasticity of recurrent excitation in the Xenopus optic tectum. Nat. Neurosci. 11, 467–475 (2008).

    CAS  Article  Google Scholar 

  37. 37

    Holt, C.E. & Harris, W.A. Order in the initial retinotectal map in Xenopus: a new technique for labeling growing nerve fibres. Nature 301, 150–152 (1983).

    CAS  Article  Google Scholar 

  38. 38

    Froemke, R.C. & Dan, Y. Spike timing–dependent synaptic modification induced by natural spike trains. Nature 416, 433–438 (2002).

    CAS  Article  Google Scholar 

  39. 39

    Sjöström, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149–1164 (2001).

    Article  Google Scholar 

  40. 40

    Wulff, P. et al. Synaptic inhibition of Purkinje cells mediates consolidation of vestibulo-cerebellar motor learning. Nat. Neurosci. 12, 1042–1049 (2009).

    CAS  Article  Google Scholar 

  41. 41

    Akerman, C.J. & Cline, H.T. Refining the roles of GABAergic signaling during neural circuit formation. Trends Neurosci. 30, 382–389 (2007).

    CAS  Article  Google Scholar 

  42. 42

    Pavlov, I., Riekki, R. & Taira, T. Synergistic action of GABAA and NMDA receptors in the induction of long-term depression in glutamatergic synapses in the newborn rat hippocampus. Eur. J. Neurosci. 20, 3019–3026 (2004).

    Article  Google Scholar 

  43. 43

    Wang, D.D. & Kriegstein, A.R. GABA regulates excitatory synapse formation in the neocortex via NMDA receptor activation. J. Neurosci. 28, 5547–5558 (2008).

    CAS  Article  Google Scholar 

  44. 44

    Hensch, T.K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508 (1998).

    CAS  Article  Google Scholar 

  45. 45

    Nieuwkoop, P.D. & Faber, J. Normal Table of Xenopus laevis (Daudin): A Systematical and Chronological Survey of the Development from the Fertilized Egg till the End of Metamorphosis (North-Holland Pub., Amsterdam, 1967).

  46. 46

    Khawaled, R., Bruening-Wright, A., Adelman, J.P. & Maylie, J. Bicuculline block of small-conductance calcium-activated potassium channels. Pflugers Arch. 438, 314–321 (1999).

    CAS  Article  Google Scholar 

  47. 47

    Niell, C.M. & Smith, S.J. Functional imaging reveals rapid development of visual response properties in the zebrafish tectum. Neuron 45, 941–951 (2005).

    CAS  Article  Google Scholar 

  48. 48

    Dayan, P. & Abbott, L.F. Neural encoding I: firing rates and spike statistics. in Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems (eds. Sejnowski, T.J. & Poggio, T.) 3–44 (MIT Press, Cambridge, Massachusetts, 2003).

  49. 49

    Song, S., Miller, K.D. & Abbott, L.F. Competitive Hebbian learning through spike timing–dependent synaptic plasticity. Nat. Neurosci. 3, 919–926 (2000).

    CAS  Article  Google Scholar 

  50. 50

    Tao, H.W., Zhang, L.I., Engert, F. & Poo, M. Emergence of input specificity of LTP during development of retinotectal connections in vivo. Neuron 31, 569–580 (2001).

    CAS  Article  Google Scholar 

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Acknowledgements

We would like to thank H. Cline, K. Lamsa and O. Paulsen for helpful discussions and for comments on the manuscript. This work was supported by grants from the Biotechnology and Biological Sciences Research Council (BB/E0154761) and the Medical Research Council (G0601503). The research leading to these results has received funding from the European Research Council under the European Community's Seventh Framework Programme (FP7/2007-2013), ERC grant agreement number 243273. In addition, C.J.A. was supported by a Fellowship from the Research Councils UK and British Pharmacological Society, and B.A.R. was supported by a Wellcome Trust Doctoral Fellowship and a Post Graduate Scholarship from the Natural Sciences and Engineering Research Council of Canada.

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B.A.R. conducted the experiments. B.A.R., O.P.V. and C.J.A. designed the experiments, contributed to the data analysis, prepared the figures and wrote the manuscript.

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Correspondence to Colin J Akerman.

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Richards, B., Voss, O. & Akerman, C. GABAergic circuits control stimulus-instructed receptive field development in the optic tectum. Nat Neurosci 13, 1098–1106 (2010). https://doi.org/10.1038/nn.2612

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