Sensitive Periods in the Development of the Brain and Behavior
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Sensitive Periods in the Development of the Brain and Behavior Eric I. Knudsen Abstract & Experience exerts a profound influence on the brain and, tecture of a circuit in fundamental ways, causing certain pat- therefore, on behavior. When the effect of experience on the terns of connectivity to become highly stable and, therefore, brain is particularly strong during a limited period in energetically preferred. Plasticity that occurs beyond the end development, this period is referred to as a sensitive period. of a sensitive period, which is substantial in many circuits, Such periods allow experience to instruct neural circuits to alters connectivity patterns within the architectural constraints process or represent information in a way that is adaptive for established during the sensitive period. Preferences in a cir- the individual. When experience provides information that is cuit that result from experience during sensitive periods are essential for normal development and alters performance illustrated graphically as changes in a ‘‘stability landscape,’’ a permanently, such sensitive periods are referred to as critical metaphor that represents the relative contributions of genetic periods. and experiential influences in shaping the information pro- Although sensitive periods are reflected in behavior, they cessing capabilities of a neural circuit. By understanding sen- are actually a property of neural circuits. Mechanisms of plas- sitive periods at the circuit level, as well as understanding the ticity at the circuit level are discussed that have been shown relationship between circuit properties and behavior, we gain to operate during sensitive periods. A hypothesis is proposed a deeper insight into the critical role that experience plays in that experience during a sensitive period modifies the archi- shaping the development of the brain and behavior. & INTRODUCTION changes in brain function. The identification of critical Learning that occurs during sensitive periods lays the periods is of particular importance to clinicians, because foundation for future learning. A classical example is that the adverse effects of atypical experience throughout a of filial imprinting (Lorenz, 1937): During a limited critical period cannot be remediated by restoring typical period soon after birth, a young animal (mammal or experience later in life. The period for filial imprinting, bird) learns to recognize, and bonds with, its parent for example, is a critical period. (Hess, 1973). The newborn cannot know the identity of Most of us view sensitive and critical periods from the its parent a priori, so it imprints on the individual that is perspective of behavior. Many aspects of our perceptual, consistently nearby and that satisfies best its innate cognitive, and emotional capabilities are shaped power- expectations for the characteristics of a parent. Under fully by experiences we have during limited periods in unusual conditions, that individual may not even be of life. For example, the capacity to perceive stereoscopic the same species. The learning that occurs during this depth requires early experience with fused binocular sensitive period exerts a long-lasting influence on the vision (Crawford, Harwerth, Smith, & von Noorden, development of the individual’s social and emotional 1996; Jampolsky, 1978); the capacity to process a lan- behavior (Immelmann, 1972; Scott, 1962). guage proficiently requires early exposure to the lan- The term ‘‘sensitive period’’ is a broad term that guage (Newport, Bavelier, & Neville, 2001; Weber-Fox & applies whenever the effects of experience on the brain Neville, 1996; Kuhl, 1994; Oyama, 1976); and the capac- are unusually strong during a limited period in develop- ities to form strong social relationships and exhibit ment. Sensitive periods are of interest to scientists and typical responses to stress require early positive inter- educators because they represent periods in develop- actions with a primary care giver (Thompson, 1999; Liu ment during which certain capacities are readily shaped et al., 1997; Leiderman, 1981; Hess, 1973). In each case, or altered by experience. Critical periods are a special the experience must be of a particular kind and it must class of sensitive periods that result in irreversible occurwithinacertainperiodifthebehavioristo develop normally. Although sensitive periods are reflected in behavior, Stanford University School of Medicine they are actually a property of neural circuits. Because D 2004 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 16:8, pp. 1412–1425 behavior results from information that has been pro- certain other species. Song learning is associated with cessed through hierarchies of neural circuits, behavioral architectural and functional changes in a forebrain measures tend to underestimate the magnitude and nucleus (the lateral magnocellular nucleus of the ante- persistence of the effects of early experience on neural rior neostriatum) which is essential for song learning circuits. Therefore, to define sensitive periods and to (Doupe, 1997; Wallhausser-Franke, Nixdorf-Bergweiler, explore why they occur and how they might be manipu- & DeVoogd, 1995; Bottjer, Meisner, & Arnold, 1984). For lated, we must think about them at the level of circuits. some species, song learning occurs only during a limited period early in development, whereas for others song learning continues throughout life. Examples of Sensitive Periods Auditory processing of spatial information in the To illustrate properties of sensitive periods, I will re- midbrain of the barn owl is an example of a sensitive fer primarily to data from four systems that have been period that is not a critical period. The processing of studied in some detail: the systems for (1) ocular rep- auditory spatial information in barn owls exhibits an resentation in the cortex of mammals, (2) auditory space unusually high degree of plasticity in juvenile animals processing in the midbrain of barn owls, (3) filial im- (Knudsen, 2002). A circuit in the external nucleus of the printing in the forebrain of ducks and chickens, and (4) inferior colliculus, integrates information from various song learning in the forebrain of songbirds. The fol- localization cues and forms associations between audi- lowing is a brief introduction to each of these systems. tory cue values and locations in space. Neural connec- Ocular representation in the primary visual cortex of tivity is shaped powerfully by juvenile experience, as the monkeys, cats, and ferrets is the most thoroughly studied circuit calibrates its representations of auditory cues to of all systems that exhibit a sensitive period (Katz & Shatz, create a map of space that is accurate for the individual. 1996; Daw, 1994; Fox & Zahs, 1994; Shatz & Stryker, 1978; Manipulations of the owl’s hearing or vision (vision Hubel & Wiesel, 1977). In this circuit, information origi- calibrates the representation of auditory cues in this nating from either the left or right eye is conveyed to circuit) during the juvenile period result in the acquisi- cortical layer IV by axons from the thalamus. The con- tion of highly atypical representations of auditory cue nections of thalamic axons with neurons in layer IV are values. However, typical representations of cue values shaped powerfully by visual experience during the first can be acquired even after the juvenile period ends by months after birth. During this period, chronic closure of restoring normal hearing and vision, and by providing one eyelid (monocular deprivation) causes a selective the owl with a sufficiently rich environment (Brainard & elimination of connections from the closed eye and an Knudsen, 1998). Because of this last property, this elaboration of new connections from the open eye period is not a critical period. (Antonini & Stryker, 1993). As a result, the circuit in layer IV comes to be dominated by input from the open eye. Opening of Sensitive Periods After the period ends, the typical pattern of ocular representation cannot be recovered despite the restora- Initial Conditions tion of visual input to both eyes (Wiesel & Hubel, 1965). Not all circuits are shaped during sensitive periods. In Because of this last property, ocular representation in the some circuits, the connectivity (pattern and strengths of visual cortex is an example of a critical period. connections) that exists in the mature circuit is estab- Filial imprinting in ducks and chickens is another lished by innate mechanisms with essentially no contri- example of a critical period. Within a few days of hatch- bution from experience (Figure 1A). This is the case for ing, these animals imprint on auditory and visual stimuli many circuits that are located near the sensory or motor that identify the parent (Bolhuis & Honey, 1998; Ramsay periphery, such as in the retina or the spinal cord, or that & Hess, 1954). Imprinting causes neurons in a particular operate automatically (Kania & Jessell, 2003; Dyer & nucleus in the forebrain (the intermediate and medial Cepko, 2001; Meissirel, Wikler, Chalupa, & Rakic, 1997). hyperstriatum ventrale) to undergo changes in architec- Other circuits maintain a high degree of plasticity ture and biochemistry and to become functionally se- throughout life, such as in the basolateral nucleus of lective for the imprinted stimulus (Horn, 1998, 2004; the amygdala, the molecular layer of the cerebellar cortex, Scheich, 1987). After the imprinting period ends, the or the CA1 region of the hippocampus