Abstract
Visual deprivation during a developmental sensitive period markedly alters visual cortical response properties, but the changes in intracortical circuitry that underlie these effects are poorly understood. Here we use a slice preparation of rat primary visual cortex to show that 2 d of prior visual deprivation early in life increases the excitability of layer 4 circuitry. Slice recordings showed that spontaneous activity of layer 4 star pyramidal neurons increased 25-fold after 2 d of visual deprivation between postnatal days (P) 15 and P17. This effect was mediated by increased net excitatory and decreased net inhibitory synaptic drive. Paired recordings showed that excitatory connections between star pyramidal neurons doubled in amplitude, whereas inhibitory connections decreased or increased depending on the interneuron class. These effects reversed when vision was restored. This dynamic adjustment of the excitation-inhibition balance may allow the networks within layer 4 to maintain stable levels of activity in the face of variable sensory input.
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References
Hubel, D.H. & Wiesel, T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond.) 206, 419–436 (1970).
Shatz, C.J. & Stryker, M.P. Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J. Physiol. (Lond.) 281, 267–283 (1978).
Shatz, C.J. Impulse activity and the patterning of connections during CNS development. Neuron 5, 745–756 (1990).
Gordon, J.A. & Stryker, M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16, 3274–3286 (1996).
Benevento, L.A., Bakkum, B.W., Port, J.D. & Cohen, R.S. The effects of dark-rearing on the electrophysiology of the rat visual cortex. Brain Res. 572, 198–207 (1992).
Heynen, A.J. et al. Molecular mechanism for loss of visual cortical responsiveness following brief monocular deprivation. Nat. Neurosci. 6, 854–862 (2003).
Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 34, 709–720 (1994).
White, L.E., Coppola, D.M. & Fitzpatrick, D. The contribution of sensory experience to the maturation of orientation selectivity in ferret visual cortex. Nature 411, 1049–1052 (2001).
Taha, S. & Stryker, M.P. Rapid ocular dominance plasticity requires cortical but not geniculate protein synthesis. Neuron 34, 425–436 (2002).
Trachtenberg, J.T., Trepel, C. & Stryker, M.P. Rapid extragranular plasticity in the absence of thalamocortical plasticity in the developing primary visual cortex. Science 287, 2029–2032 (2000).
van Sluyters, R.C. Reversal of the physiological effects of brief periods of monocular deprivation in the kitten. J. Physiol. (Lond.) 284, 1–17 (1978).
Maurer, D., Lewis, T.L., Brent, H.P. & Levin, A.V. Rapid improvement in the acuity of infants after visual input. Science 286, 108–110 (1999).
Peters, A. & Kara, D.A. The neuronal composition of area 17 of rat visual cortex. I. The pyramidal cells. J. Comp. Neurol. 234, 218–241 (1985).
Martin, K.A. Microcircuits in visual cortex. Curr. Opin. Neurobiol. 12, 418–425 (2002).
Kawaguchi, Y. & Kubota, Y. GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb. Cortex 7, 476–486 (1997).
Peters, A. & Kara, D.A. The neuronal composition of area 17 of rat visual cortex. II. The nonpyramidal cells. J. Comp. Neurol. 234, 242–263 (1985).
Desai, N.S., Cudmore, R.H., Nelson, S.B. & Turrigiano, G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat. Neurosci. 5, 783–789 (2002).
Hendry, S.H. & Jones, E.G. Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753 (1986).
Benevento, L.A., Bakkum, B.W. & Cohen, R.S. γ-Aminobutyric acid and somatostatin immunoreactivity in the visual cortex of normal and dark-reared rats. Brain Res. 689, 172–182 (1995).
Reid, S.N. & Juraska, J.M. The cytoarchitectonic boundaries of the monocular and binocular areas of the rat primary visual cortex. Brain Res. 563, 293–296 (1991).
Zilles, K., Wree, A., Schleicher, A. & Divac, I. The monocular and binocular subfields of the rat's primary visual cortex: a quantitative morphological approach. J. Comp. Neurol. 226, 391–402 (1984).
Caleo, M., Lodovichi, C., Pizzorusso, T. & Maffei, L. Expression of the transcription factor Zif268 in the visual cortex of monocularly deprived rats: effects of nerve growth factor. Neuroscience 91, 1017–1026 (1999).
Worley, P.F. et al. Constitutive expression of zif268 in neocortex is regulated by synaptic activity. Proc. Natl Acad. Sci. USA 88, 5106–5110 (1991).
Chutkow, J. Metabolism of magnesium in central nervous system. Relationship between concentrations of magnesium in cerebrospinal fluid and brain in magnesium deficiency. Neurology 24, 780–787 (1974).
Zhang, E.T., Hansen, A.J., Wieloch, T. & Lewitzen, M. Influence of MK-801 on brain extracellular calcium and potassium activities in severe hypoglicemia. J. Cereb. Blood Flow Metab. 10, 136–139 (1990).
Sanchez-Vives, M.V. & McCormick, D. Cellular and network mechanisms of rhythmic recurrent activity in neocortex. Nat. Neurosci. 3, 1027–1034 (2000).
Desai, N.S., Rutherford, L.C. & Turrigiano, G.G. Plasticity in the intrinsic excitability of cortical pyramidal neurons. Nat. Neurosci. 2, 515–520 (1999).
Turrigiano, G.G., Leslie, K.R., Desai, N.S., Rutherford, L.C. & Nelson, S.B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892–896 (1998).
Kilman, V., van Rossum, M.C. & Turrigiano, G.G. Activity deprivation reduces miniature IPSC amplitude by decreasing the number of postsynaptic GABA(A) receptors clustered at neocortical synapses. J. Neurosci. 22, 1328–1337 (2002).
Finnerty, G.T. & Connors, B.W. Sensory deprivation without competition yields modest alterations of short-term synaptic dynamics. Proc. Natl Acad. Sci. USA 97, 12864–12868 (2000).
Finnerty, G.T., Roberts, L.S. & Connors, B.W. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400, 367–371 (1999).
O'Brien, R.J. et al. Activity-dependent modulation of synaptic AMPA receptor accumulation. Neuron 21, 1067–1078 (1998).
DeFelipe, J. Cortical interneurons: from Cajal to 2001. Prog. Brain Res. 136, 215–238 (2002).
Rutherford, L.C., DeWan, A., Lauer, H.M. & Turrigiano, G.G. Brain-derived neurotrophic factor mediates the activity-dependent regulation of inhibition in neocortical cultures. J. Neurosci. 17, 4527–4535 (1997).
Morales, B., Choi, S.Y. & Kirkwood, A. Dark rearing alters the development of GABAergic transmission in visual cortex. J. Neurosci. 22, 8084–8090 (2002).
Shao, Z. & Burkhalter, A. Different balance of excitation and inhibition in feed-forward and feedback circuits of rat visual cortex. J. Neurosci. 16, 7353–7365 (1996).
Hajos, F., Staiger, J.F., Halasy, K., Freund, T.F. & Zilles, K. Geniculo-cortical afferents form synaptic contacts with vasoactive intestinal polypeptide (VIP) immunoreactive neurons of the rat visual cortex. Neurosci. Lett. 228, 179–182 (1997).
Miller, K.D. Synaptic economics: competition and cooperation in synaptic plasticity. Neuron 17, 371–374 (1996).
Abbott, L.F. & Nelson, S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. 3, 1178–1183 (2000).
Turrigiano, G.G. & Nelson, S.B. Homeostatic plasticity in the developing nervous system. Nat. Rev. Neurosci. 5, 97–107 (2004).
Hendry, S.H., Fuchs, J., deBlas, A.L. & Jones, E.G. Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J. Neurosci. 10, 2438–2450 (1990).
Meineke, D.L. & Peters, A. GABA immunoreactive neurons in rat visual cortex. J. Comp. Neurol. 261, 388–404 (1987).
Kirkwood, A. & Bear, M.F. Hebbian synapses in visual cortex. J. Neurosci. 14, 1634–1645 (1994).
Hensch, T.K. et al. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282, 1504–1508 (1998).
Huang, Z.J. et al. BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell 98, 739–755 (1999).
Chagnac-Amitai, Y. & Connors, B.W. Horizontal spread of synchronized activity in neocortex and its control by GABA-mediated inhibition. J. Neurophysiol. 61, 747–758 (1989).
Sjostrom, P.J., Turrigiano, G.G. & Nelson, S.B. Rate, timing, and cooperativity jointly determine cortical synaptic plasticity. Neuron 32, 1149–1164 (2001).
Deuchars, J. & Thomson, A.M. Single axon fast inhibitory postsynaptic potentials elicited by a sparsely spiny interneuron in rat neocortex. Neuroscience 65, 935–942 (1995).
Peters, A. & Herrimann, K.M. Enigmatic bipolar cell of rat visual cortex. J. Comp. Neurol. 267, 409–432 (1988).
Beierlein, M., Gibson, J.R. & Connors, B.W. Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J. Neurophysiol. 90, 2987–3000 (2003).
Acknowledgements
We thank R. Cudmore for help with software, J. Barry and K. Essig for histology and S. Fusi and X.-J. Wang for helpful discussions. Supported by the National Eye Institute (EY014439) and the National Institute on Drug Abuse (DA16455).
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Supplementary Fig. 1
Reconfiguration of layer 4 connectivity by visual deprivation. Diagram illustrates the circuitry in Control (left) and Deprived (right) layer 4. Deprivation increases the amplitude (thick red axons) and connection probability of excitatory synapses between layer 4 star pyramids. In contrast, the amplitude of inhibitory connections from FS interneurons onto star pyramids was reduced in amplitude (dashed green axons). Finally, inhibitory connections from RSNP neurons onto star pyramids increased in amplitude (thick blue axon) but connection probability was cut in half. These changes should act to boost recurrent excitation within layer 4, while reducing feedback inhibition from FS neurons and leaving feed-forward inhibition roughly constant. (PDF 268 kb)
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Maffei, A., Nelson, S. & Turrigiano, G. Selective reconfiguration of layer 4 visual cortical circuitry by visual deprivation. Nat Neurosci 7, 1353–1359 (2004). https://doi.org/10.1038/nn1351
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DOI: https://doi.org/10.1038/nn1351
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