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• W2014906957 abstract "Changes of ocular dominance in the visual cortex can be induced by visual manipulations during a critical period in early life. However, the role of critical period plasticity in normal development is unknown. Here we show that at the onset of this time window, the preferred orientations of individual cortical cells in the mouse are mismatched through the two eyes and the mismatch decreases and reaches adult levels by the end of the period. Deprivation of visual experience during this period irreversibly blocks the binocular matching of orientation preference, but has no effect in adulthood. The critical period of binocular matching can be delayed by long-term visual deprivation from birth, like that of ocular dominance plasticity. These results demonstrate that activity-dependent changes induced by normal visual experience during the well-studied critical period serve to match eye-specific inputs in the cortex, thus revealing a physiological role for critical period plasticity during normal development. Changes of ocular dominance in the visual cortex can be induced by visual manipulations during a critical period in early life. However, the role of critical period plasticity in normal development is unknown. Here we show that at the onset of this time window, the preferred orientations of individual cortical cells in the mouse are mismatched through the two eyes and the mismatch decreases and reaches adult levels by the end of the period. Deprivation of visual experience during this period irreversibly blocks the binocular matching of orientation preference, but has no effect in adulthood. The critical period of binocular matching can be delayed by long-term visual deprivation from birth, like that of ocular dominance plasticity. These results demonstrate that activity-dependent changes induced by normal visual experience during the well-studied critical period serve to match eye-specific inputs in the cortex, thus revealing a physiological role for critical period plasticity during normal development. Orientation preference of cortical neurons is binocularly mismatched in young mice Binocular matching of orientation preference takes place during the critical period Binocular matching requires normal visual experience and NMDA receptor activation Visual deprivation from birth delays the critical period of binocular matching Optimal functioning of the nervous system requires selective wiring of neural circuits, the precision of which is achieved through experience-dependent refinement after birth (Katz and Shatz, 1996Katz L.C. Shatz C.J. Synaptic activity and the construction of cortical circuits.Science. 1996; 274: 1133-1138Crossref PubMed Scopus (2269) Google Scholar). The necessity of experience in neural systems development is often studied by depriving or manipulating sensory experiences (Feldman and Brecht, 2005Feldman D.E. Brecht M. Map plasticity in somatosensory cortex.Science. 2005; 310: 810-815Crossref PubMed Scopus (413) Google Scholar, Hensch, 2004Hensch T.K. Critical period regulation.Annu. Rev. Neurosci. 2004; 27: 549-579Crossref PubMed Scopus (824) Google Scholar, Knudsen and Brainard, 1995Knudsen E.I. Brainard M.S. Creating a unified representation of visual and auditory space in the brain.Annu. Rev. Neurosci. 1995; 18: 19-43Crossref PubMed Scopus (117) Google Scholar). In the visual system, for example, following a period of monocular visual deprivation (MD) in juvenile animals, cortical neurons lose their responses to the deprived eye and become more responsive to the nondeprived eye (Wiesel and Hubel, 1963Wiesel T.N. Hubel D.H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body.J. Neurophysiol. 1963; 26: 978-993PubMed Google Scholar). Such MD-induced anatomical and physiological changes, referred to as ocular dominance (OD) plasticity, are largely restricted to a critical period in early life (Gordon and Stryker, 1996Gordon J.A. Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.J. Neurosci. 1996; 16: 3274-3286PubMed Google Scholar, Hubel and Wiesel, 1970Hubel D.H. Wiesel T.N. The period of susceptibility to the physiological effects of unilateral eye closure in kittens.J. Physiol. 1970; 206: 419-436PubMed Google Scholar, Issa et al., 1999Issa N.P. Trachtenberg J.T. Chapman B. Zahs K.R. Stryker M.P. The critical period for ocular dominance plasticity in the Ferret's visual cortex.J. Neurosci. 1999; 19: 6965-6978PubMed Google Scholar, Wiesel and Hubel, 1965Wiesel T.N. Hubel D.H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens.J. Neurophysiol. 1965; 28: 1029-1040PubMed Google Scholar). Decades of studies have made OD plasticity and its critical period a classical model of experience-dependent neural development (Hensch, 2004Hensch T.K. Critical period regulation.Annu. Rev. Neurosci. 2004; 27: 549-579Crossref PubMed Scopus (824) Google Scholar). These studies, especially those after the mouse was established as a model system for OD plasticity (Gordon and Stryker, 1996Gordon J.A. Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.J. Neurosci. 1996; 16: 3274-3286PubMed Google Scholar), have provided important knowledge of the regulation of critical period timing and of synaptic changes induced by MD (Hensch, 2005Hensch T.K. Critical period plasticity in local cortical circuits.Nat. Rev. Neurosci. 2005; 6: 877-888Crossref PubMed Scopus (1402) Google Scholar). Despite these exciting advances, a fundamental question still remains unanswered: what purpose does this period of heightened plasticity serve during normal development? The critical period of OD plasticity overlaps with the normal maturation of visual acuity (Cancedda et al., 2004Cancedda L. Putignano E. Sale A. Viegi A. Berardi N. Maffei L. Acceleration of visual system development by environmental enrichment.J. Neurosci. 2004; 24: 4840-4848Crossref PubMed Scopus (201) Google Scholar, Fagiolini et al., 1994Fagiolini 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. 1994; 34: 709-720Crossref PubMed Scopus (511) Google Scholar, Movshon and Van Sluyters, 1981Movshon J.A. Van Sluyters R.C. Visual neural development.Annu. Rev. Psychol. 1981; 32: 477-522Crossref PubMed Scopus (281) Google Scholar) and MD was shown to decrease visual acuity (Boothe et al., 1985Boothe R.G. Kiorpes L. Carlson M.R. Studies of strabismus and amblyopia in infant monkeys.J. Pediatr. Ophthalmol. Strabismus. 1985; 22: 206-212PubMed Google Scholar, Prusky and Douglas, 2003Prusky G.T. Douglas R.M. Developmental plasticity of mouse visual acuity.Eur. J. Neurosci. 2003; 17: 167-173Crossref PubMed Scopus (136) Google Scholar). However, the relationship between visual acuity increase in normal development and OD plasticity is unclear. This is because OD plasticity is only induced by an imbalance of inputs from the two eyes, a condition that does not exist in normal visual system development. In fact, the degree of cortical OD does not change during the critical period unless the system is manipulated experimentally (Sato and Stryker, 2008Sato M. Stryker M.P. Distinctive features of adult ocular dominance plasticity.J. Neurosci. 2008; 28: 10278-10286Crossref PubMed Scopus (171) Google Scholar). In other words, while the critical period marks a period of increased cortical plasticity during development, functional cortical changes that normally take place during this time window are not known. Presumably, visual experience during the critical period induces synaptic changes that are important for normal cortical development. We set out to determine what cortical function is shaped by such normal-vision-induced plasticity. Two major transformations occur when visual information reaches the cortex. In addition to binocularity, cortical cells are also selective for stimulus orientation (Ferster and Miller, 2000Ferster D. Miller K.D. Neural mechanisms of orientation selectivity in the visual cortex.Annu. Rev. Neurosci. 2000; 23: 441-471Crossref PubMed Scopus (479) Google Scholar, Hubel and Wiesel, 1962Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154PubMed Google Scholar). Binocular cells in the cortex must then match their orientation tuning through the two eyes in order for the animal to perceive coherently. Indeed, in cats and primates, the preferred orientations of cortical neurons are similar through the two eyes (Bridge and Cumming, 2001Bridge H. Cumming B.G. Responses of macaque V1 neurons to binocular orientation differences.J. Neurosci. 2001; 21: 7293-7302PubMed Google Scholar, Ferster, 1981Ferster D. A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex.J. Physiol. 1981; 311: 623-655PubMed Google Scholar, Hubel and Wiesel, 1962Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154PubMed Google Scholar, Nelson et al., 1977Nelson J.I. Kato H. Bishop P.O. Discrimination of orientation and position disparities by binocularly activated neurons in cat straite cortex.J. Neurophysiol. 1977; 40: 260-283PubMed Google Scholar). How, then, is the binocularly matched orientation preference established? We hypothesize that the heightened plasticity during the critical period allows visual experience to drive the binocular matching of orientation preference during normal development. For this to be true, the following criteria have to be met. (1) The preferred orientations of individual cortical neurons should be mismatched between the two eyes in young animals. (2) The binocular similarity of orientation preference should improve and reach adult levels during the critical period. (3) Alterations in visual experience during the critical period, but not in adulthood, should disrupt the binocular matching. (4) Abnormal matching induced by visual deprivation in juvenile animals should not recover with subsequent visual experience. In this study, we have tested and confirmed each of these predictions in mice. Our results thus demonstrate that activity-dependent changes induced by normal visual experience during the critical period serve to match eye-specific inputs in the cortex. By ascribing a physiological role for critical period plasticity during normal development, our discovery therefore opens new areas of research in the study of experience-dependent visual system development. We first examined the binocular relationship of orientation preference in adult mice between P60 and P90, well after the critical period for OD plasticity. Single-unit recordings were made with microelectrodes in the binocular zone of the primary visual cortex (V1). The orientation tuning properties of each neuron were determined separately for each eye in response to drifting sinusoidal gratings of varying orientations. The neuron in Figures 1A and 1B, for example, was tuned to nearly identical orientations through the two eyes (only 3° difference). Such similarity in the preferred orientations between the two eyes was observed across the population (Figure 1C, correlation coefficient r = 0.86 and p < 0.0001, n = 75). In adult mice, the difference in orientation preference between the two eyes (their absolute values are hereafter referred to as “ΔO”) was smaller than 20° in most cells (Figure 1D), with a median of 10.4° and a mean of 19.7° ± 2.6° (Table 1). These results indicate that the orientation preference of individual cortical neurons is closely matched between the two eyes, consistent with studies in cats and primates (Bridge and Cumming, 2001Bridge H. Cumming B.G. Responses of macaque V1 neurons to binocular orientation differences.J. Neurosci. 2001; 21: 7293-7302PubMed Google Scholar, Ferster, 1981Ferster D. A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex.J. Physiol. 1981; 311: 623-655PubMed Google Scholar, Hubel and Wiesel, 1962Hubel D.H. Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.J. Physiol. 1962; 160: 106-154PubMed Google Scholar, Nelson et al., 1977Nelson J.I. Kato H. Bishop P.O. Discrimination of orientation and position disparities by binocularly activated neurons in cat straite cortex.J. Neurophysiol. 1977; 40: 260-283PubMed Google Scholar).Table 1Quantitative Analysis of Binocular Matching and Orientation Tuning in Different Experimental GroupsMean ΔOMean OSIMean OS WidthAll cellsOSI > 0.33OSI > 0.50Median ΔOContraIpsiContraIpsiNumber of miceP20–P2330.1° ± 3.0° (n = 80)25.7° ± 3.3° (n = 59)24.7° ± 4.1° (n = 46)27.5° (n = 80)0.68 ± 0.04 (n = 80)0.66 ± 0.03 (n = 80)27.5° ± 1.8° (n = 39)28.6° ± 2.0° (n = 39)n = 16P31–P3617.0° ± 1.7° (n = 100)13.6° ± 1.5° (n = 73)11.6° ± 1.4° (n = 59)11.0° (n = 100)0.69 ± 0.03 (n = 100)0.70 ± 0.03 (n = 100)25.4° ± 1.9° (n = 49)27.5° ± 1.7° (n = 49)n = 15P60–P9019.7° ± 2.6° (n = 75)16.9° ± 2.6° (n = 67)14.2° ± 2.4° (n = 55)10.4° (n = 75)0.76 ± 0.03 (n = 75)0.75 ± 0.03 (n = 75)28.1° ± 1.6° (n = 53)26.7° ± 1.6° (n = 53)n = 18DR (P24 to P31–P36)29.6° ± 3.0° (n = 68)26.5° ± 3.3° (n = 50)24.8° ± 3.6° (n = 39)27.6° (n = 68)0.68 ± 0.04 (n = 68)0.68 ± 0.03 (n = 68)26.0° ± 1.9° (n = 31)27.7° ± 2.1° (n = 31)n = 7MD31.4° ± 3.5° (n = 56)30.2° ± 3.8° (n = 49)30.0° ± 4.1° (n = 40)24.3° (n = 56)0.76 ± 0.04 (n = 56)0.74 ± 0.04 (n = 56)30.5° ± 2.2° (n = 24)28.6° ± 2.4° (n = 24)n = 8NMDAR suppression28.6° ± 2.9° (n = 67)27.2° ± 3.1° (n = 57)25.6° ± 3.3° (n = 47)20.3° (n = 67)0.76 ± 0.03 (n = 67)0.74 ± 0.03 (n = 67)25.2° ± 1.9° (n = 33)23.7° ± 1.8° (n = 33)n = 8Saline control18.0° ± 2.2° (n = 65)17.4° ± 2.3° (n = 56)15.5° ± 2.5° (n = 47)12.6° (n = 65)0.77 ± 0.03 (n = 65)0.76 ± 0.03 (n = 65)25.2° ± 1.9° (n = 41)27.5° ± 2.1° (n = 41)n = 7MD recovery29.0° ± 3.6° (n = 56)23.8° ± 3.7° (n = 39)22.6° ± 4.6° (n = 29)20.1° (n = 56)0.68 ± 0.04 (n = 56)0.66 ± 0.04 (n = 56)31.1° ± 2.1° (n = 28)26.8° ± 1.6° (n = 28)n = 6Adult MD20.5° ± 2.9° (n = 50)16.4° ± 2.6° (n = 42)12.7° ± 1.8° (n = 31)14.5° (n = 50)0.69 ± 0.04 (n = 50)0.77 ± 0.04 (n = 50)27.6° ± 2.0° (n = 30)26.6° ± 1.8° (n = 30)n = 8DR (P0–P31) 0 Day38.6° ± 3.7° (n = 56)35.7° ± 4.1° (n = 47)37.0° ± 4.8° (n = 34)34.3° (n = 56)0.72 ± 0.03 (n = 56)0.68 ± 0.03 (n = 56)31.3° ± 2.2° (n = 23)34.1° ± 2.0° (n = 23)n = 6DR (P0–P31) 6–7 Day21.0° ± 2.7° (n = 58)17.8° ± 2.8° (n = 49)14.6° ± 2.6° (n = 43)12.4° (n = 58)0.80 ± 0.03 (n = 58)0.77 ± 0.04 (n = 58)31.0° ± 1.9° (n = 35)27.2° ± 1.9° (n = 35)n = 4 Open table in a new tab We next quantified the degree of orientation selectivity of individual neurons by calculating an Orientation Selectivity Index (OSI; see Experimental Procedures for details). The vast majority of binocular neurons in adult mice are orientation selective. In fact, 89% of the cells (n = 67/75) had an OSI greater than 0.33 for both eyes (a 2:1 response ratio for the preferred orientation over its orthogonal), and 73% (n = 55/75) had an OSI greater than 0.5 (a 3:1 ratio). The mean OSI was equally high to the two eyes (contralateral: 0.76 ± 0.03, ipsilateral: 0.75 ± 0.03). These values are similar to those in a recent report of monocular neurons in adult mice (Niell and Stryker, 2008Niell C.M. Stryker M.P. Highly selective receptive fields in mouse visual cortex.J. Neurosci. 2008; 28: 7520-7536Crossref PubMed Scopus (590) Google Scholar). Importantly, most cortical cells had OSIs similar to that of the two eyes (Figure 1E, r = 0.60 and p < 0.0001). We also calculated an Ocular Dominance Index (ODI, ranging from −1 to 1, where positive values indicate contralateral bias and negative values indicate ipsilateral bias). These cells had a mean ODI of 0.19 ± 0.03, confirming the contralateral bias in the binocular zone of the mouse visual cortex (Cang et al., 2005Cang J. Kalatsky V.A. Löwel S. Stryker M.P. Optical imaging of the intrinsic signal as a measure of cortical plasticity in the mouse.Vis. Neurosci. 2005; 22: 685-691Crossref PubMed Scopus (103) Google Scholar, Gordon and Stryker, 1996Gordon J.A. Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.J. Neurosci. 1996; 16: 3274-3286PubMed Google Scholar). Finally, we determined orientation tuning width, linearity, and preferred spatial frequency of these cells and found that they were all binocularly similar (Figures 1F, 1G, and S1, available online). Although the orientation preferences are well matched binocularly in adulthood, we found that they are mismatched early during postnatal development. Two time periods were chosen in our study (Figure 2A), P20–P23 and P31–P36, to correspond to the onset and offset, respectively, of the critical period for OD plasticity (Gordon and Stryker, 1996Gordon J.A. Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.J. Neurosci. 1996; 16: 3274-3286PubMed Google Scholar). In mice between P20–P23, many cells were tuned to quite different orientations through the two eyes. For some cells (e.g., Figures 2B and 2C), the preferred orientations through the two eyes were nearly 90° apart, the maximum possible difference. Overall, many more cells at this age had greater ΔO than in adult mice (compare Figure 2D with Figure 1D). At P20–P23, 50% of the cells had a ΔO value of more than 27.5° (i.e., median = 27.5°, mean = 30.1° ± 3.0°, n = 80), significantly greater than in adult (median = 10.4°, mean = 19.7° ± 2.6°; p < 0.01; Figures 2F and 2G), indicating that orientation preference is significantly mismatched binocularly in the young mice. The mismatch decreases with age (Figures 2E–2G and S2A) and reaches adult levels by P31–P36 (median = 11.0°, mean = 17.0° ± 1.7°, n = 100; p < 0.001 compared to P20–P23, and p = 0.76 compared to adults). One important consideration is that the larger ΔO in younger animals may be due to a potential difference in eye alignment. The symmetrical, zero-centered histograms of the difference in preferred orientations (Figure 2D) suggested this to be unlikely, but they included multiple animals. We therefore compared the relative orientation between the two eyes in individual mice by optical imaging of cortical retinotopic maps (Figures 3A and 3B). We determined the angle of rotation between the monocularly obtained contralateral and ipsilateral maps. This angle, which reflects the relative rotation between the two eyes, was similar in juvenile and adult mice (Figure 3C), ruling out the possibility of a different eye alignment in younger mice, whether it be a developmental phenomenon or an experimental artifact. The development of binocular matching of orientation preference (i.e., decrease in ΔO) may be due to an increase in orientation selectivity, as less selective cells appeared to have a slightly larger ΔO (Figure S3). To address this possibility, we first limited our analysis of ΔO to orientation selective cells. When only selective (OSI > 0.33 to both eyes) or highly selective (OSI > 0.5) cells were included, the ΔO in P20–P23 mice was still significantly higher than that in the older animals (Figure 4B). These results indicate that in young mice, even cells that are highly orientation selective through both eyes are binocularly mismatched in their preferred orientations. Next, we examined directly the developmental profile of orientation tuning. Individual tuning curves of all cells were normalized and shifted to their max responses, and then averaged to be compared across development. These curves were indistinguishable across the three age groups (Figures 4C and 4D). Furthermore, we also quantified the OSI and tuning width of individual cells and found that both of them were nearly identical between P20–P23 and P31–P36 (Figures 4E and 4F and Table 1). The OSI increased only slightly in adult mice (Figure 4E). Together, these analyses indicate that by P20 cortical cells have acquired basic features of orientation selectivity monocularly, and the preferred orientations are then matched binocularly in a subsequent stage of visual system development. To determine whether the binocular matching we have just discovered requires normal visual experience, we used two types of manipulations: dark rearing (DR) and MD (Figure 5A). A short period of DR during the critical period deprives the animal of any visual input, which is known to have no effect on OD. In contrast, MD alters the balance of input between the two eyes and induces OD plasticity (Fagiolini et al., 1994Fagiolini 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. 1994; 34: 709-720Crossref PubMed Scopus (511) Google Scholar, Gordon and Stryker, 1996Gordon J.A. Stryker M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse.J. Neurosci. 1996; 16: 3274-3286PubMed Google Scholar, Issa et al., 1999Issa N.P. Trachtenberg J.T. Chapman B. Zahs K.R. Stryker M.P. The critical period for ocular dominance plasticity in the Ferret's visual cortex.J. Neurosci. 1999; 19: 6965-6978PubMed Google Scholar, Wiesel and Hubel, 1963Wiesel T.N. Hubel D.H. Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body.J. Neurophysiol. 1963; 26: 978-993PubMed Google Scholar). For binocular matching, however, both manipulations blocked the developmental decrease of ΔO. The distributions of ΔO in both DR (from P24 to P31–P36, mean of 29.6° ± 3.0° and median of 27.6°) and MD (from P24 to P31–P32, mean of 31.4° ± 3.5° and median of 24.3°) groups were similar to those of P20–P23 mice (Figure 5B), but greater than those of their age-matched controls (P31–36), This difference held true for analyses with all cells, selective cells, and highly selective cells (Figure 5C). Brief DR and MD resulted in no change in orientation selectivity (Figure 5D). Therefore, normal visual experience between P24–P31 is required for the binocular matching of orientation preference. While a previous report showed that common input from the two eyes was not necessary for binocular matching of large-scale orientation columns (Gödecke and Bonhoeffer, 1996Gödecke I. Bonhoeffer T. Development of identical orientation maps for two eyes without common visual experience.Nature. 1996; 379: 251-254Crossref PubMed Scopus (125) Google Scholar), our results provide evidence for experience-dependent binocular matching at the single-cell level. The above experiments demonstrate that normal visual experience induces cortical changes to match binocular orientation preference. The binocular matching process is presumably driven by the correlated neuronal activity between the eye-specific inputs to individual cortical neurons. Because the NMDA receptor is known as a coincidence detector in synaptic plasticity (Bourne and Nicoll, 1993Bourne H.R. Nicoll R. Molecular machines integrate coincident synaptic signals.Cell. 1993; 72: 65-75Abstract Full Text PDF PubMed Scopus (184) Google Scholar), we examined whether its activation is required for the binocular matching process. Systemic administration of the competitive NMDA receptor antagonist (R,S)-3-(2-carboxypiperazin-4-yl)propyl-1-phosphonic acid (CPP) was shown recently to block MD-induced OD changes in both juvenile and adult mice, but have no effect on OD in normally reared animals (Sato and Stryker, 2008Sato M. Stryker M.P. Distinctive features of adult ocular dominance plasticity.J. Neurosci. 2008; 28: 10278-10286Crossref PubMed Scopus (171) Google Scholar). Following the established protocol, we injected CPP intraperitoneally (i.p.) into normally reared mice starting from P24–P25, with repeated injections every ∼24 hr for 7–9 days (Figure 5E). These mice were recorded about 24 hr after the last injection. At P31–P33, their ΔO (28.6° ± 2.9°, n = 67) was still close to those of P20–P23 mice (Table 1) and significantly higher than that of the saline-injected controls (18.0° ± 2.2°, n = 65) (Figure 5F). The difference held true for analyses with only selective and highly selective cells (Table 1, p < 0.05). Importantly, the pharmacological manipulation did not alter cortical orientation selectivity (both OSI and tuning width, see Figure 5G and Table 1), consistent with the finding that these monocular tuning properties have already established by the onset of the critical period (Figure 4). Together, these experiments indicate that NMDA-receptor-dependent synaptic plasticity, presumably driven by normal visual experience, take place in the critical period during normal development to match binocular orientation preference. We next studied whether the period of heightened cortical plasticity, often revealed in the study of OD plasticity, is also “critical” for the binocular matching of orientation preference. If visual experience during this time window is truly crucial for the establishment of binocular matching, the disrupted matching induced by visual manipulation will not be able to recover, even after normal visual experience is restored after the critical period. To test this, we monocularly deprived mice at P24 and reopened the closed eye at P31–P32 (Figure 6A). After approximately 1 month of normal visual experience following the MD, the ΔO in these mice (mean of 29.0° ± 3.6°) was still close to those immediately after MD (31.4° ± 3.5°), and significantly higher than that of normal adult mice (19.7° ± 2.6°, p < 0.05; Figure 6B and Table 1), indicating no recovery for the disrupted binocular matching of orientation preference. A number of recent studies have shown that OD plasticity persists into adulthood in mice (Hofer et al., 2006Hofer S.B. Mrsic-Flogel T.D. Bonhoeffer T. Hübener M. Prior experience enhances plasticity in adult visual cortex.Nat. Neurosci. 2006; 9: 127-132Crossref PubMed Scopus (172) Google Scholar, Pham et al., 2004Pham T.A. Graham S.J. Suzuki S. Barco A. Kandel E.R. Gordon B. Lickey M.E. A semi-persistent adult ocular dominance plasticity in visual cortex is stabilized by activated CREB.Learn. Mem. 2004; 11: 738-747Crossref PubMed Scopus (108) Google Scholar, Sato and Stryker, 2008Sato M. Stryker M.P. Distinctive features of adult ocular dominance plasticity.J. Neurosci. 2008; 28: 10278-10286Crossref PubMed Scopus (171) Google Scholar, Sawtell et al., 2003Sawtell N.B. Frenkel M.Y. Philpot B.D. Nakazawa K. Tonegawa S. Bear M.F. NMDA receptor-dependent ocular dominance plasticity in adult visual cortex.Neuron. 2003; 38: 977-985Abstract Full Text Full Text PDF PubMed Scopus (353) Google Scholar), questioning the concept of the critical period. We therefore investigated the effect of MD on binocular matching in adulthood and found that 7–8 days of MD in adult mice (Figure 6A) had no effect on binocular matching of orientation preference, where ΔO (mean of 20.5° ± 2.9°, n = 50) remains similar to that of normal adult controls (Figure 6B and Table 1; p = 0.16). These two sets of experiments therefore demonstrate the existence of a critical period for binocular matching of orientation preference: visual experience in this period, but not after this period, is crucially needed for the normal development of cortical binocularity. DR from birth is known to delay the critical period of OD plasticity (Cynader and Mitchell, 1980Cynader M. Mitchell D.E. Prolonged sensitivity to monocular deprivation in dark-reared cats.J. Neurophysiol. 1980; 43: 1026-1040PubMed Google Scholar, Fagiolini et al., 2003Fagiolini M. Katagiri H. Miyamoto H. Mori H. Grant S.G. Mishina M. Hensch T.K. Separable features of visual cortical plasticity revealed by N-methyl-D-aspartate receptor 2A signaling.Proc. Natl. Acad. Sci. USA. 2003; 100: 2854-2859Crossref PubMed Scopus (138) Google Scholar). We therefore studied whether the binocular matching of orientation preference can be similarly delayed by such long-term visual deprivation. The above experiments have demonstrated that the critical period of binocular matching normally closes by P31, because the disrupted matching cannot recover with subsequent visual experience. We thus reared mice in constant darkness from birth to P31 and then switched to a normal light-dark cycle to examine whether the binocular matching of orientation preference can still be achieved (Figure 7A). A normal level of orientation tuning was observed immediately after DR, for OSI (Table 1), tuning width (Table 1), and mean tuning curves (Figures 7E and 7F), consistent with a previous study in mice using DR of similar duration (Iwai et al., 2003Iwai Y. Fagiolini M. Obata K. Hensch T.K. Rapid critical period induction by tonic inhibition in visual cortex.J. Neurosci. 2003; 23: 6695-6702PubMed Google Scholar). Importantly, this result provided an opportunity to determine the degree of binocular matching achieved in the absence of any visual experience, which is difficult to study in normal development because of the technical difficulty in recording from very young mice. Overall, cortical neurons were tuned to very different orientations through the two eyes immediately after DR (Figure 7B; ΔO: mean of 38.6° ± 3.7° and median of 34.3°, n = 56). In fact, the distribution of ΔO (Figure 7C) was not statistically different from random binocular matching, which would have been a uniform distribution (p = 0.07, one sample Kolmogorov-Smirnov [K-S] test). This suggests that binocular matching of orientation preference is likely achieved entirely by experience-" @default.
• W2014906957 created "2016-06-24" @default.
• W2014906957 creator A5058259205 @default.
• W2014906957 creator A5063733171 @default.
• W2014906957 creator A5066162010 @default.
• W2014906957 date "2010-01-01" @default.
• W2014906957 modified "2023-10-10" @default.
• W2014906957 title "Critical Period Plasticity Matches Binocular Orientation Preference in the Visual Cortex" @default.
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