Sensitive Periods in the Development of the
Brain and Behavior
Eric I. Knudsen
& Experience exerts a profound influence on the brain and,
therefore, on behavior. When the effect of experience on the
brain is particularly strong during a limited period in
development, this period is referred to as a sensitive period.
Such periods allow experience to instruct neural circuits to
process or represent information in a way that is adaptive for
the individual. When experience provides information that is
essential for normal development and alters performance
permanently, such sensitive periods are referred to as critical
Although sensitive periods are reflected in behavior, they
are actually a property of neural circuits. Mechanisms of plas-
ticity at the circuit level are discussed that have been shown
to operate during sensitive periods. A hypothesis is proposed
that experience during a sensitive period modifies the archi-
tecture of a circuit in fundamental ways, causing certain pat-
terns of connectivity to become highly stable and, therefore,
energetically preferred. Plasticity that occurs beyond the end
of a sensitive period, which is substantial in many circuits,
alters connectivity patterns within the architectural constraints
established during the sensitive period. Preferences in a cir-
cuit that result from experience during sensitive periods are
illustrated graphically as changes in a ‘‘stability landscape,’’ a
metaphor that represents the relative contributions of genetic
and experiential influences in shaping the information pro-
cessing capabilities of a neural circuit. By understanding sen-
sitive periods at the circuit level, as well as understanding the
relationship between circuit properties and behavior, we gain
a deeper insight into the critical role that experience plays in
shaping the development of the brain and behavior. &
Learning that occurs during sensitive periods lays the
foundation for future learning. A classical example is that
of filial imprinting (Lorenz, 1937): During a limited
period soon after birth, a young animal (mammal or
bird) learns to recognize, and bonds with, its parent
(Hess, 1973). The newborn cannot know the identity of
its parent a priori, so it imprints on the individual that is
consistently nearby and that satisfies best its innate
expectations for the characteristics of a parent. Under
unusual conditions, that individual may not even be of
the same species. The learning that occurs during this
sensitive period exerts a long-lasting influence on the
development of the individual’s social and emotional
behavior (Immelmann, 1972; Scott, 1962).
The term ‘‘sensitive period’’ is a broad term that
applies whenever the effects of experience on the brain
are unusually strong during a limited period in develop-
ment. Sensitive periods are of interest to scientists and
educators because they represent periods in develop-
ment during which certain capacities are readily shaped
or altered by experience. Critical periods are a special
class of sensitive periods that result in irreversible
changes in brain function. The identification of critical
periods is of particular importance to clinicians, because
the adverse effects of atypical experience throughout a
critical period cannot be remediated by restoring typical
experience later in life. The period for filial imprinting,
for example, is a critical period.
Most of us view sensitive and critical periods from the
perspective of behavior. Many aspects of our perceptual,
cognitive, and emotional capabilities are shaped power-
fully by experiences we have during limited periods in
life. For example, the capacity to perceive stereoscopic
depth requires early experience with fused binocular
vision (Crawford, Harwerth, Smith, & von Noorden,
1996; Jampolsky, 1978); the capacity to process a lan-
guage proficiently requires early exposure to the lan-
guage (Newport, Bavelier, & Neville, 2001; Weber-Fox &
Neville, 1996; Kuhl, 1994; Oyama, 1976); and the capac-
ities to form strong social relationships and exhibit
typical responses to stress require early positive inter-
actions with a primary care giver (Thompson, 1999; Liu
et al., 1997; Leiderman, 1981; Hess, 1973). In each case,
the experience must be of a particular kind and it must
occur within a certain period if the behavior is to
Although sensitive periods are reflected in behavior,
they are actually a property of neural circuits. Because
Stanford University School of Medicine
D 2004 Massachusetts Institute of TechnologyJournal of Cognitive Neuroscience 16:8, pp. 1412–1425
behavior results from information that has been pro-
cessed through hierarchies of neural circuits, behavioral
measures tend to underestimate the magnitude and
persistence of the effects of early experience on neural
circuits. Therefore, to define sensitive periods and to
explore why they occur and how they might be manipu-
lated, we must think about them at the level of circuits.
Examples of Sensitive Periods
To illustrate properties of sensitive periods, I will re-
fer primarily to data from four systems that have been
studied in some detail: the systems for (1) ocular rep-
resentation in the cortex of mammals, (2) auditory space
processing in the midbrain of barn owls, (3) filial im-
printing in the forebrain of ducks and chickens, and (4)
song learning in the forebrain of songbirds. The fol-
lowing is a brief introduction to each of these systems.
Ocular representation in the primary visual cortex of
monkeys, cats, and ferrets is the most thoroughly studied
ofallsystemsthatexhibit asensitiveperiod (Katz&Shatz,
1996;Daw,1994; Fox&Zahs,1994; Shatz&Stryker,1978;
Hubel & Wiesel, 1977). In this circuit, information origi-
nating from either the left or right eye is conveyed to
cortical layer IV by axons from the thalamus. The con-
nections of thalamic axons with neurons in layer IV are
shaped powerfully by visual experience during the first
months after birth. During this period, chronic closure of
one eyelid (monocular deprivation) causes a selective
elimination of connections from the closed eye and an
elaboration of new connections from the open eye
(Antonini & Stryker, 1993). As a result, the circuit in layer
IV comes to be dominated by input from the open eye.
After the period ends, the typical pattern of ocular
representation cannot be recovered despite the restora-
tion of visual input to both eyes (Wiesel & Hubel, 1965).
Because ofthis last property, ocular representation in the
visual cortex is an example of a critical period.
Filial imprinting in ducks and chickens is another
example of a critical period. Within a few days of hatch-
ing, these animals imprint on auditory and visual stimuli
that identify the parent (Bolhuis & Honey, 1998; Ramsay
& Hess, 1954). Imprinting causes neurons in a particular
nucleus in the forebrain (the intermediate and medial
hyperstriatum ventrale) to undergo changes in architec-
ture and biochemistry and to become functionally se-
lective for the imprinted stimulus (Horn, 1998, 2004;
Scheich, 1987). After the imprinting period ends, the
preference for the imprinted stimulus does not change
with subsequent experience.
Song memorization in songbirds occurs during a
critical period in some species but throughout life in
other closely related species. Songbirds memorize the
song that they will sing (Konishi, 1985; Marler, 1970a).
Normally, they learn the song of their father (when only
the male sings). However, in the absence of a father’s
song, they will learn other song dialects or the songs of
certain other species. Song learning is associated with
architectural and functional changes in a forebrain
nucleus (the lateral magnocellular nucleus of the ante-
rior neostriatum) which is essential for song learning
(Doupe, 1997; Wallhausser-Franke, Nixdorf-Bergweiler,
& DeVoogd, 1995; Bottjer, Meisner, & Arnold, 1984). For
some species, song learning occurs only during a limited
period early in development, whereas for others song
learning continues throughout life.
Auditory processing of spatial information in the
midbrain of the barn owl is an example of a sensitive
period that is not a critical period. The processing of
auditory spatial information in barn owls exhibits an
unusually high degree of plasticity in juvenile animals
(Knudsen, 2002). A circuit in the external nucleus of the
inferior colliculus, integrates information from various
localization cues and forms associations between audi-
tory cue values and locations in space. Neural connec-
tivity is shaped powerfully by juvenile experience, as the
circuit calibrates its representations of auditory cues to
create a map of space that is accurate for the individual.
Manipulations of the owl’s hearing or vision (vision
calibrates the representation of auditory cues in this
circuit) during the juvenile period result in the acquisi-
tion of highly atypical representations of auditory cue
values. However, typical representations of cue values
can be acquired even after the juvenile period ends by
restoring normal hearing and vision, and by providing
the owl with a sufficiently rich environment (Brainard &
Knudsen, 1998). Because of this last property, this
period is not a critical period.
Opening of Sensitive Periods
Not all circuits are shaped during sensitive periods. In
some circuits, the connectivity (pattern and strengths of
connections) that exists in the mature circuit is estab-
lished by innate mechanisms with essentially no contri-
bution from experience (Figure 1A). This is the case for
many circuits that are located near the sensory or motor
periphery, such as in the retina or the spinal cord, or that
operate automatically (Kania & Jessell, 2003; Dyer &
Cepko, 2001; Meissirel, Wikler, Chalupa, & Rakic, 1997).
Other circuits maintain a high degree of plasticity
throughout life, such as in the basolateral nucleus of
or the CA1 region of the hippocampus (Medina, Christo-
pher Repa, Mauk, & LeDoux, 2002; Malenka & Nicoll,
1999; Ito, 1984). In these circuits, the range of potential
throughout the lifetime of the animal (Figure 1B).
Most circuits operate between these extremes. For
these circuits, innate influences establish an initial pat-
tern of connectivity that is preferred (a valley in the
stability landscape; Figure 1C), but the pattern is not
specified precisely. This kind of circuit may be shaped by
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