A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex Shigeru Tanaka*, Toshiki Tani, Je´ roˆ me Ribot¤a, Kazunori O’Hashi¤b, Kazuyuki Imamura¤c Laboratory for Visual Neurocomputing, RIKEN Brain Science Institute, Wako, Saitama, Japan Abstract Orientation selectivity of primary visual cortical neurons is an important requisite for shape perception. Although numerous studies have been previously devoted to a question of how orientation selectivity is established and elaborated in early life, how the susceptibility of orientation plasticity to visual experience changes in time remains unclear. In the present study, we showed a postnatal sensitive period profile for the modifiability of orientation selectivity in the visual cortex of kittens reared with head-mounted goggles for stable single-orientation exposure. When goggle rearing (GR) started at P16-P30, 2 weeks of GR induced a marked over-representation of the exposed orientation, and 2 more weeks of GR consolidated the altered orientation maps. GR that started later than P50, in turn, induced the under-representation of the exposed orientation. Orientation plasticity in the most sensitive period was markedly suppressed by cortical infusion of NMDAR antagonist. The present study reveals that the plasticity and consolidation of orientation selectivity in an early life are dynamically regulated in an experience-dependent manner. Citation: Tanaka S, Tani T, Ribot J, O’Hashi K, Imamura K (2009) A Postnatal Critical Period for Orientation Plasticity in the Cat Visual Cortex. PLoS ONE 4(4): e5380. doi:10.1371/journal.pone.0005380 Editor: Georges Chapouthier, L’universite´ Pierre et Marie Curie, France Received January 29, 2009; Accepted March 23, 2009; Published April 29, 2009 Copyright: 2009 Tanaka et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This study was partly supported by a Grant-in-Aid for Scientific Research (19300141; the funder’s website: http://www.jsps.go.jp/english/index.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: shigeru@riken.jp ¤a Current address: Laboratoire de Physiologie de la Perception et de l’Action, UMR 7150, Colle`ge de France-CNRS, Paris, France ¤b Current address: Department of Neurobiology, Weizmann Institute of Science, Rehovot, Israel ¤c Current address: Department of Systems Life Engineering, Maebashi Institute of Technology, Gunma, Japan Introduction Neuronal circuits in the mammalian visual cortex maintain certain dynamic mechanisms of structural and functional modi- fication in the early postnatal period as well as in adulthood. Typically, monocular deprivation in early postnatal days leads to a shift in the dominant responses of primary visual cortical neurons to the non-deprived, experienced eye [1–4]. A deficit of vision caused by retinal damage is compensated for by rewiring of cortical circuits even in adult animals [5]. A different type of plasticity has been found with regard to the orientation selectivity of visual cortical neurons: it is currently thought that the orientation selectively is innately generated [6], and then maintained [7] and elaborated [8] by visual experience in early postnatal days. Experimentally, this orientation plasticity is induced by exposure of young animals to retinal images restricted to a single orientation [9–16]. However, results to date are variable, reflecting the various methods used for inducing and detecting the orientation plasticity. This variability has made it difficult to delineate the postnatal critical period during which orientation plasticity manifests. Recent technological progress in optical imaging of intrinsic signals [17–21] and data processing methods for noise reduction [22,23] now provide an efficient method, complementary to conventional unit recording, for revealing overall features of the cortical distribution of orientation selectivity. In addition, head- mounted cylindrical-lens-fitted goggles [24] provide an efficient tool for restricting visual experience to a single orientation. We previously reported that attaching goggles to a kitten continuously without interruption by dark-rearing episodes was particularly effective in causing modification of orientation selectivity [15]. In this study, we used these technical improvements to determine the critical period for orientation plasticity in cat primary visual cortex. It has been shown that infusion of an NMDA receptor antagonist to the visual cortex suppresses the expression of orientation selectivity [25,26]. It is further expected that NMDA-receptor-mediated long-term potentiation (LTP) at synapses to visual cortical neurons optimally activated by the exposed orientation is involved in the over-representation of that orientation. We confirmed that cortical infusion of an NMDA receptor antagonist nearly abolished the modifiability of orienta- tion selectivity during the critical period. We also addressed an important question of how the orientation map modified by single- orientation exposure is consolidated afterwards. Results Normal rearing Figure 1 shows three orientation polar maps (Figs. 1a, c and e) and corresponding orientation histograms (Figs. 1b, d and f), obtained from normally reared kittens of different ages. At P29, the relative size of responsive domains is largest for horizontal orientation (0u or equivalently 180u) and smallest for vertical orientation (90u) (Fig. 1b). The sample-averaged orientation histogram across 10 normally reared kittens in the age range of P26–32 exhibited a bias toward horizontal orientation (Fig. S1a PLoS ONE | www.plosone.org 1 April 2009 | Volume 4 | Issue 4 | e5380