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Critical Periods Revisited: Plasticity of Sensory Systems

Critical Periods Revisited


In domains as diverse as vision, language, social imprinting, and recovery from brain damage, there is evidence that the brain goes through critical periods of development during childhood that restrict the influence of experience. Against the mass of evidence for critical periods, however, is a small recent literature revealing remarkable residual cortical plasticity in adults.

A September 24, 2007, meeting of the Academy's Imaging Discussion Group focused on critical periods in brain development and adult plasticity in the context of the visual system. J. Anthony Movshon (New York University), Brian Wandell (Stanford University), Charles Gilbert (The Rockefeller University), and Takao Hensch (Harvard University) presented pioneering work on the specific mechanisms of experience-dependent changes linked to adult learning and structural damage, as well as the complex mechanisms that drive and regulate critical periods. This eBriefing also includes summaries of presentations by Len Press (Family Eyecare Associates) and Susan Barry (Mount Holyoke College).

Journal Articles

Sensitive Periods in Visual Development

Blakemore C, Van Sluythers RC. 1974. Reversal of the physiological effects of monocular deprivation in kittens: further evidence for a sensitive period. J. Physiol. 237: 195-216. (PDF, 2.1 MB) Full Text

Distler C, Bachevalier J, Kennedy C, et al. 1996. Functional development of the corticocortical pathway for motion analysis in the macaque monkey: a 14C-2-deoxyglucose study. Cereb. Cortex. 6: 184-195. (PDF, 6.2 MB) Full Text

Hubel DH, Wiesel TN. 1970. The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. 206: 419-436. (PDF, 3.24 MB) Full Text

Harwerth RS, Smith EL 3rd, Duncan GC, et al. 1986. Multiple sensitive periods in the development of the primate visual system. Science 232: 235-238.

Kiorpes L, Bassin SA. 2003. Development of contour integration in macaque monkeys. Vision Neurosci. 20: 567-575.

Kiorpes L, Gavlin A, El-Shamayleh Y. 2006. Perception of texture in macaque monkeys: development and amblyopia. Program No. 604.8. 2006 Neuroscience Meeting Planner. Atlanta, GA: Society for Neuroscience.

Kiorpes L, Movshon JA. 2004. Development of sensitivity to visual motion in macaque monkeys. Vis. Neurosci. 21: 851-859.

Kiorpes L, Movshon JA. 1998. Peripheral and central factors limiting the development of contrast sensitivity in macaque monkeys. Vision Res. 38: 61-70.

Kiorpes L, Stavros KA. 2006. Development of temporal contrast sensitivity in monkeys. Perception 35 ECVP Abstract Supplement.

Kiorpes L, Tang C, Hawken MJ, Movshon JA. 2003. Ideal observer analysis of the development of spatial contrast sensitivity in macaque monkeys. J. Vis. 3: 630-641.

Kovacs I, Kozma P, Feher A, Benedek G. 1999. Late maturation of visual spatial integration in humans. Proc. Natl. Acad. Sci. USA 96: 12204-12209. Full Text

Mishkin M, Ungerleider LG. 1982. Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortec in monkeys. Behav. Brain Res. 6: 57-77.

Movshon JA, Adelson EH, Gizzi MS, Newsome WT. The analysis of moving visual patterns. In Chagas C, Gattass R, Gross C, eds. 1985. Pattern Recognition Mechanisms (Pontificiae Academiae Scientiarum Scripta Varia 54, 117-151). Vatican Press, Rome. (Reprinted in Experimental Brain Research, Supplementum 11, 117-151, 1986, and in Kosslyn SM, Andersen RA, eds. 1992. Frontiers in Cognitive Neuroscience. MIT Press, Cambridge, MA).

Movshon JA, Kiorpes L, Hawken MJ, Cavanaugh JR. 2005. Functional maturation of the macaques's lateral geniculate nucleus. J. Neurosci. 25: 2712-2722. Full Text

Movshon JA, Rust NC, Kohn A, et al. 2003. Receptive field properties of MT neurons in infant macaques. Society for Neuroscience Abstracts 2003, 126.8. Society for Neuroscience, Washington, DC.

Price T, Kiorpes L, Movshon JA. 2004. Differential development of form and motion perception in macaque monkeys. Society for Neuroscience, San Diego, 2004.

Critical Periods in Human Development

Flege J, Bohn, O-S, Jang S. 1997. Effects of experience on non-native speakers' production and perception of English vowels. J. Phonetics 25: 437-470.

Hannon E, Trehub S. 2006. Tuning into musical rhythms: Infants learn more readily than adults. Proc. Natl. Acad. Sci. USA 102: 12639-12643. Full Text

Lewis TL, Maurer D. 2005. Multiple sensitive periods in human visual development: Evidence from visually deprived children. Dev. Psychobiol. 46: 163-183.

Michel GF, Tyler AN. 2005. Critical period: a history of the transition from questions of when, to what to how. Dev. Psychobiol. 48: 326-331.

Sharma A, Dorman M, Kral A. 2005. The influence of a sensitive period on central auditory development in children with unilateral and bilateral cochlear implants. Hear. Res. 203: 134-143.

Stiles J, Reilly J, Paul B, Moses P. 2005. Cognitive development following brain injury: evidence for neural adaptation. Trends Cog. Sci. 9: 136-143. (PDF, 389 KB) Full Text

Werker J, Tees R. 2005. Speech perception as a window for understanding plasticity and commitment in language systems of the brain. Dev. Psychobiol. 46: 233-251.

Evidence for Plasticity after the Critical Period

Levi D. 2005. Perceptual learning in adults with amblyopia: a reevaluation of critical periods in human vision. Dev. Psychobiol. 46: 222-232.

Green C, Bavelier D. 2003. Action video game modifies visual selective attention. Nature 423: 534-537.

McLelland J, Fiez J, McCandliss B. 2002. Teaching the /r/-/l/ discrimination to Japanese adults: behavioral and neural aspects. Physiol. Behav. 77: 657-662.

Pascual-Leone A, Hamilton R. 2001. The metamodal organization of the brain. Prog. Brain Res. 134: 427-445.

Sangrigoli S, Pallier C, Argenti A, et al. 2005. Reversibility of the other-race effect in face recognition during childhood. Psychol. Sci. 16: 440-444.

Ventureyra V, Pallier C, Yoo H. 2004. The loss of first language phonetic perception in adopted Koreans. J. Neurolinguistics 17: 79-91. (PDF, 121 KB) Full Text

The Human Visual Pathways: Maps and Plasticity

Brewer AA, Liu J, Wade AR, Wandell BA. 2005. Visual field maps and stimulus selectivity in human ventral occipital cortex. Nat. Neurosci. 8: 1102-1109.

Fine I, Wade AR, Brewer AA, et al. 2003. Long-term deprivation affects visual perception and cortex. Nat. Neurosci. 6: 915-916.

Masuda Y, Nakadomari S, Dumoulin SO, et al. 2007. The mechanism underlying large-scale reorganization in human macular degeneration patients. J. Vision 7: 230.

Stelios M, Smirnakis AA, Brewer MC, et al. 2005. Lack of long-term cortical reorganization after macaque retinal lesions. Nature 435: 300-307.

Wandell B, Brewer AA, Dougherty RF. 2005. Visual field map clusters in human cortex. Philos. Trans. R Soc. London B Biol. Sci. 360: 693-707. Full Text

Learning to See: Neural Mechanisms of Perceptual Learning

Darian-Smith C, Gilbert CD. 1994. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368: 737-740.

Li W , Piech V , Gilbert CD. 2006. Contour saliency in primary visual cortex. Neuron 50: 951-962.

Li W, Piëch V, Gilbert CD. 2004. Perceptual learning and top-down influences in primary visual cortex. Nat. Neurosci. 7: 651-657. Full Text

Li W, Gilbert CD. 2002. Global contour saliency and local colinear interactions. J. Neurophysiol. 88: 2846-2856. Full Text

Obata S, Obata J, Das A, Gilbert CD. 1999. Molecular correlates of topographic reorganization in primary visual cortex following retinal lesions. Cereb. Cortex 9: 238-248. Full Text

Porter PB. 1954. Another picture puzzle. Am. J. Psychol. 67: 550–551.

Sigman M, Cecchi GA, Gilbert CD, Magnasco MO. 2001. On a common circle: natural scenes and Gestalt rules. Proc. Natl. Acad. Sci. USA 98: 1935-1940. Full Text

Stettler DD, Das A, Bennett J, Gilbert CD. Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36: 739-750.

Stettler DD, Yamahachi H, Li W, et al. 2006. Axons and synaptic boutons are highly dynamic in adult visual cortex. Neuron 49: 877-887.

Unlocking Brakes on Plasticity

Fagiolini M, Fritschy JM, Löw K, et al. 2004. Specific GABAA circuits for visual cortical plasticity. Science 303: 1681-1683.

Hensch TK. 2005. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6: 877-888.

Hensch TK. 2005. Recovery in the blink of an eye. Neuron 48: 166-168.

Hensch TK, Fagiolini M. 2005. Excitatory-inhibitory balance and critical period plasticity in developing visual cortex. Prog. Brain Res. 147: 115-124.

Hensch TK, Fagiolini M, Mataga N, et al. 1998. Local GABA circuit control of experience-dependent plasticity in developing visual cortex. Science 282: 1504-1508.

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

Katagiri H, Fagiolini M, Hensch TK. 2007. Optimization of somatic inhibition at critical period onset in mouse visual cortex. Neuron 53: 805-812.

Mataga N, Mizuguchi Y, Hensch TK. 2004. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44: 1031-1041.

Möhler H, Fritschy JM, Crestani F, et al. 2004. Specific GABA(A) circuits in brain development and therapy. Biochem. Pharmacol. 68: 1685-1690.

Binocularity, Critical Periods, and the Natural History of Esotropia

Barry SR, Mims JL 3rd. 2006. Regaining binocular stereoscopic vision in adulthood. A case report. A neurologist's notebook: Stereo Sue. Why two eyes are better than one. Binocul. Vis. Strabismus. Q. 21: 199-202.

Birch EE, Shimojo S, Held R. 1985. Preferential-looking assessment of fusion and steropsis in infants aged 1–6 months. Invest. Ophthalmol. Vis. Sci. 26: 366-370. (PDF, 586 KB) Full Text

McColl SL, Mitchell DE. 1998. Stereodeficient subjects show substantial differences in interocular transfer of two motion adaptation aftereffects. Vision Res. 38: 1889-1900.

Nelson JI. 1981. A neurophysiological model for anomalous correspondence based on mechanisms of sensory fusion. Doc. Ophthalmol. 31: 51-100.

Sireteanu R, Fronius M, Singer W. 1981. Binocular interactions in the peripheral visual field of humans with strabismic and anisometropic amblyopia. Vision Res. 21: 1065-1074.

Smith EL, Chino YM, Ni J, et al. 1997. Residual binocular interactions in the striate cortex of monkeys reared with abnormal binocular vision. J. Neurophysiol. 78: 1353-1362. Full Text

Stager DR, Birch EE. 1986. Preferential-looking acuity and steropsis in infantile esotropia. J. Ped. Ophthalmol. & Strabismus. 23: 160-165.

Von Noorden GK. 1996. Binocular Vision and Ocular Motility. Mosby, St. Louis, MO.


J. Anthony Movshon, PhD

New York University
e-mail | web site | publications

Anthony Movshon is professor of neural science and psychology at New York University, with an adjunct appointment at the NYU School of Medicine. His research concerns the function and development of the primate visual system, especially the visual areas of the cerebral cortex. Specifically, he analyzes the functional properties of neurons in the extrastriate visual areas of the macacque monkey's cerebral cortex to correlate relationships between visual signals and decision making, and looks at abnormal early development as a cause of amblyopia. Movshon completed his doctorate at Cambridge University in 1975, where he studied visual neurophysiology and psychophysics, and joined the faculty at New York University that same year.

Brian A. Wandell, PhD

Stanford University
e-mail | web site | publications

Brian Wandell is the first Isaac and Madeline Stein Family Professor at Stanford University. He joined the Stanford faculty in 1979, and is chair of the Psychology Department and a member, by courtesy, of the Department of Electrical Engineering and Radiology. His research projects center on how we see, spanning topics from the organization of human visual cortex, to reading development in children, to digital imaging devices and algorithms. Wandell was elected to the U.S. National Academy of Sciences in 2003 and named Electronic Imaging Scientist of the Year by the SPIE/IS&T in 2007.

Charles Gilbert, MD, PhD

The Rockefeller University
e-mail | web site | publications

Charles Gilbert is the Arthur and Janet Ross Professor of Neuroscience at the Rockefeller University. He received his MD–PhD degree from Harvard Medical School. He is a member of the National Academy of Sciences, a fellow of the American Academy of Arts and Sciences, and a member at large of the section on neuroscience of the American Association for the Advancement of Science. His work has focused on the brain mechanisms of visual perception and learning. He studies the way in which the brain analyzes visual images, and how this analysis is shaped by experience and by higher order cognitive influences. A major focus of his work is on plasticity of the visual cortex—the way in which cortical circuitry and function changes during normal perceptual learning and during functional recovery following lesions of the central nervous system.

Takao K. Hensch, PhD

Harvard University
e-mail | web site | publications

Takao Hensch is professor of neurology at Children's Hospital Boston, Harvard Medical School and professor of molecular & cellular biology at Harvard University. He received his PhD in neuroscience from the University of California, San Francisco in 1996, following a Fulbright Fellowship (Max-Planck Institute) and completion of an MPH from the University of Tokyo. Before arriving at Harvard, he helped launch the RIKEN Brain Science Institute (Wako, Japan), where he served as group director of critical period mechanisms research. By applying cellular/molecular techniques to neural systems, his work has identified particular inhibitory circuits which orchestrate the functional and structural rewiring of connections by early sensory experience. He has won a number of awards, including the 2006 Japanese Minister of Science (MEXT) Prize and the Young Investigator Award from both the Japanese (2001 Tsukahara Prize) and U.S. Society for Neuroscience (first from overseas, 2005).

Len Press, FCOVD, FAAO

Family Eyecare Associates, Fair Lawn, NJ
e-mail | web site

Len Press is an optometric physician based in Fair Lawn, NJ. In 1994 he received the New Jersey Optometric Association's Scientific Achievement Award for his contributions to the scientific advancement of the profession of optometry. Formerly, he served as chief of the Vision Therapy Service at the State University of New York, State College of Optometry. He is currently an associate professor at S.U.N.Y. where he teaches courses on children's vision and analyzing patient data. He is a member of the associate medical staff at St. Lawrence Rehabilitation Hospital in Lawrenceville, New Jersey, a Fellow of the College of Optometrists in Vision Development and a Diplomate in Binocular Vision and Perception of the American Academy of Optometry. He is also the author of two textbooks, Clinical Pediatric Optometry and Applied Concepts in Vision Therapy.

Susan R. Barry, PhD

Mount Holyoke College
e-mail | web site | publications

Susan Barry is a professor of neurobiology in the Department of Biological Sciences at Mount Holyoke College, where she has taught since 1992. Barry brings an unusual combination of experience and expertise to writing about strabismus, stereopsis, and visual plasticity. She can draw on her neurobiological expertise to describe the neuronal mechanisms underlying the acquisition of stereovision in adulthood. At the same time, she can call on her own personal experience as well as discussions with other formerly stereoblind individuals to explain why the development of binocularity produces such profound effects. Barry received her PhD in biology from Princeton University in 1981, has authored scientific papers on the study of nerve cells, neuronal plasticity, and eye-head-hand coordination, and lectures widely on the topics of binocular vision and neuronal plasticity.