OF SENSITIVE PERIODS

We see, then, that factors such as the experience of play, characteristics of the physical environment, or changes in the animal’s nervous system or hormonal state can cause behavioral change during development. Now we will see that often these factors have their effects on development during particular windows of time, called sensitive periods.

CHANGING TERMINOLOGY—

FROM CRITICAL PERIODS TO SENSITIVE PERIODS

Early on, windows of opportunity for learning were called critical periods. Konrad Lorenz (1935) borrowed this term from embryology, where it was used to describe times in early development that were characterized by rapid changes in organization. During these brief, well-defined periods, an experimental interruption of the nor-mal sequence of events produced profound and

irreversible effects on the developing embryo. Thus, as first used by Lorenz, a critical period was a phase of sus-ceptibility to environmental stimuli that was brief, well defined, and within which exposure to certain stimuli produced irreversible effects on subsequent behavior.

Recently, terms such as sensitive period, sensitive phase, susceptible period, and optimal period have been used in place of critical period. The newer terms indeed reflect certain modifications in the definition of this period in light of more recent research (reviewed in Michel and Tyler 2005). In fact, many of Lorenz’s (1935) basic precepts have now been modified. Specifically, we now know that such periods (1) are fairly extended, (2) are not sharply defined but gradual in their onset and termination, (3) differ in duration among species, indi-viduals, and functional systems, and (4) depend on the nature and intensity of environmental stimuli both before and during the sensitive period. Moreover, most phenomena based on sensitive periods are not irre-versible. Instead, patterns of behavior developed during sensitive periods can usually be altered or suppressed under certain conditions, especially those associated with high levels of stress. Deprivation (e.g., rearing an animal in isolation or in darkness) can reverse or destroy a pattern of behavior established during a sensitive period. It is important, however, not to overemphasize the reversibility of patterns of behavior established dur-ing sensitive periods. Conditions such as reardur-ing in com-plete isolation or total darkness are unlikely to be encountered by most animals outside the laboratory environment. Furthermore, even in the laboratory, behaviors established during sensitive periods are usu-ally more resistant to change than those learned at other times (Immelmann and Suomi 1981). We will use the term sensitive period because it is now commonly found in the literature. Our working definition of sensitive period is a time during development when certain expe-riences have a greater influence on the characteristics of an individual than at other stages.

TIMING OF SENSITIVE PERIODS

In most animals, sensitive periods occur early in life.

Why is this so? We usually assume that this is the time when animals have the greatest opportunity to gain knowledge from parents and close relatives, knowledge that is particularly important in species recognition.

Later, they might not interact with them so intimately, and in some cases they will, in fact, be exposed to intense stimuli from other species (Immelmann and Suomi 1981). For example, in some species of birds, the young remain in the nest for only a few weeks after hatching and then leave to join mixed-species flocks. It would not be surprising if these young learn to recognize

con-specifics during a brief sensitive period before leaving the nest. Otherwise, choosing an appropriate mate could later be a confusing exercise indeed because birds that waited too long to learn the defining qualities of their species might very well learn the plumage and song char-acteristics of another species.

Some animals have little or no contact with their parents or other close relatives after birth or hatching.

One might wonder, then, would sensitive periods occur early in development in these species? And is early learning limited to acquiring knowledge about appro-priate social partners, or do animals also learn charac-teristics of appropriate places to live or breed? Consider the case of Pacific salmon in the genus Oncorhynchus.

Adult salmon spawn in freshwater, usually streams, and depending on the species and population, they may or may not die after spawning. When the eggs hatch and the fry eventually emerge from their gravel nests, they typically pass through several developmental stages in their home streams, the last of which, called the smolt stage, prepares them for migrating thousands of kilo-meters downstream to enter oceanic feeding grounds.

After a time at sea, virtually all surviving adults return to their natal stream to spawn. It is a remarkable feat of navigation, and when they reach the freshwater inlets, they unerringly swim up the appropriate tributaries, making all the correct decisions at every fork until they reach the very stream where they were spawned—and they seem to do it by smell. Apparently, before their migration to the sea and during a sensitive period, juve-nile salmon learn the odor of water at the site where they were spawned. The water at the natal spawning site has a unique chemical composition known as the “home stream olfactory bouquet,” or HSOB. The sensitive period for learning the HSOB seems to coincide with smoltification, the developmental transformation of young salmon from parr (freshwater residents) to smolts ready for seaward migration and life (see Chapter 7) (Carruth et al. 2002). It is also possible that the sensitive period begins somewhat earlier (Dittman and Quinn 1996). In any case, upon returning to their natal stream, adult salmon are stimulated to swim upstream by the familiar odor. Why is it important that salmon learn the precise location of their natal stream?

The answer is that each population is finely adapted to its home water, so much so that salmon experimentally introduced into other streams show a higher mortality rate than locally adapted individuals (Quinn and Dittman 1990). The period of early learning thus ensures that it is the odor of the fish’s own spawning place that is remembered (for a more detailed discussion of salmon homing, see Chapter 10). We see, then, that during sensitive periods, animals may learn the appro-priate cues, not only of conspecifics, but also of the local physical environment.

Onset of Sensitivity

It is clear that young animals have a heightened sensitiv-ity to certain environmental stimuli such as the physical appearance of a parent or the smell of a home stream.

One might ask, then, what causes this increased sensitiv-ity to certain cues? One suggestion is that the onset of sensitivity may be due both to endogenous (internal) and exogenous (external) factors (Bateson 1979). Increases in sensitivity generally begin as soon as the relevant motor and sensory capacities of the young animal are developed.

Changes in the internal state, such as fluctuations in hor-mone levels, may also influence sensitivity. Then, endogenous factors interact with environmental variables to produce the start of the sensitive period. For example, although the visual component of filial imprinting in birds (the response of newly hatched young to follow their mother; see later discussion) begins once hatchlings are able to perceive and process optical stimuli, experi-ence with light appears to interact with the internal con-ditions to initiate this particular sensitive period (e.g., Bateson 1976). Here, then, we have endogenous factors (ability of the nervous system to process optical stimuli) interacting with environmental factors (exposure to light) to produce the start of the sensitive period.

Decline in Sensitivity

Several explanations have been proposed for the termi-nation of sensitive periods (reviewed in Johnson 2005);

we consider two of them here. One explanation assumes that the decline in sensitivity is under endogenous con-trol, perhaps influenced by a maturational timetable.

According to this idea, some physiological factor, intrin-sic to the animal, ends the period of receptivity to exter-nal stimulation once a specific stage of maturation has been reached. Another explanation is based on the idea that learning is a self-terminating process. In essence, learning causes neurobiological changes that reduce plasticity and ultimately terminate the sensitive period.

An example of this idea is the proposition that learning a first language causes neurobiological changes in humans that effectively bring the sensitive period for lan-guage learning to a close. This might explain, for

exam-ple, why learning a second language later in life is often more difficult than learning the first language.

MULTIPLE SENSITIVE PERIODS

Individuals typically experience multiple sensitive peri-ods during their development (Bischof 2007). We will see that a young male songbird experiences sensitive periods during song learning. The same young bird will experience sensitive periods associated with sexual imprinting (learning the characteristics of an appropri-ate mappropri-ate; see lappropri-ater discussion). Another example of mul-tiple sensitive periods within individuals concerns visual development in humans (Lewis and Maurer 2005).

Researchers comparing visual development in visually normal children with that of children deprived of early visual experience because they were either born with cataracts or developed them later have discovered that there are different sensitive periods for different aspects of vision (e.g., visual acuity, peripheral vision, motion detection), and even within each of these aspects there may be more than one sensitive period.

SOME EXAMPLES OF SENSITIVE PERIODS IN BEHAVIORAL

DEVELOPMENT

Now that we have discussed the definition and timing of sensitive periods, and the fact that a given individual—

be it a songbird or a human—will experience multiple sensitive periods, let’s consider some examples of behav-ioral development that depend, to varying degrees, on specific experiences during a window of time.

Filial Imprinting

Anyone who has ever watched chicks in a farmyard or ducklings and goslings on a pond knows that the young generally follow their mother wherever she goes (Figure 8.9). How does such following behavior develop?

Konrad Lorenz (1935), working with newly hatched goslings, was the first to systematically study this behav-ior. In one experiment, he divided a clutch of eggs laid by a greylag goose (Anser anser) into two groups. One group was hatched by the mother, and as expected, these goslings trailed behind her. The second group was hatched in an incubator. The first moving object these goslings encountered was Lorenz, and they responded to him as they normally would to their mother. Lorenz marked the goslings so that he could determine in which group they belonged and placed them all under a box.

When the box was lifted, liberating all the goslings simultaneously, they streamed toward their respective

“parents,” normally reared goslings toward their mother and incubator-reared ones toward Lorenz. The goslings STOP AND THINK

A common strategy for restoring or enhancing popula-tions of anadromous salmonids (i.e., those that return from the sea to breed in freshwater) is to artificially rear young in hatcheries and then release them into streams with the expectation that they would eventually migrate to the sea. Given what you know about olfactory imprint-ing in salmon, how might the release be orchestrated and its timing planned to result in good return rates to fresh-water spawning grounds?

had developed a preference for characteristics associated with their “mother” and expressed this preference through their following behavior. The attachment was unfailing, and from that point on Lorenz had goslings following in his footsteps (Figure 8.10).

Because social attachment evidenced by following seemed to be immediate and irreversible, Lorenz named the process Pragung, which means, “stamping.” The English translation is “imprinting.” Used in this context, the term suggests that during the first encounter with a moving object, its image is somehow permanently stamped on the nervous system of the young animal.

We now know that at least two distinct processes are involved in the development by young birds such as chicks, ducklings, and goslings of a preference for fol-lowing their mother (studies reviewed by Bolhuis and Honey 1998; Hogan and Bolhuis 2005). In one process, a predisposition to approach objects with the general characteristics of conspecifics emerges in the young bird, even without previous exposure to a conspecific.

For example, chicks without any previous exposure to an adult conspecific or a red box preferentially approach a stuffed conspecific when given a choice between it and the red box. (This is not to say that experience is unim-portant in the development of the predisposition for conspecific characteristics. It turns out that other non-specific experiences, such as being handled or placed in a running wheel, can induce the predisposition as long as these experiences occur during the sensitive period.) In the second process, called filial imprinting, the young bird learns, through exposure to its mother, her particular characteristics and then preferentially follows her. The biological function of filial imprinting is prob-ably to allow young birds to recognize close relatives and thereby distinguish their parents from other adults that might attack them (Bateson 1990). The two processes—development of the predisposition and filial imprinting—seem to be localized in different regions of the brain. We will focus our discussion on the develop-ment of the following response in mallard ducklings.

FIGURE8.9 Young Canada geese follow-ing their mother. The followfollow-ing response results from filial imprinting, the process by which young precocial birds learn the characteristics of their mother and then preferentially follow her.

FIGURE8.10 Goslings following their

“mother,” Konrad Lorenz. Lorenz was one of the first scientists to study imprinting experimentally.

Mallard ducklings, like most young in the orders Anseriformes (ducks, geese, and swans) and Galliformes (chickens, turkeys, and quail), are precocial, that is, quite capable of moving about and feeding on their own just a short time after hatching. Filial imprinting is usually studied in species with precocial young. The following response is nonexistent—or much less evident—in species such as the songbirds discussed later, whose young are altricial, that is, virtually helpless and incapable of feeding on their own or following their parents for the first few weeks after hatching. We begin with a brief description of reproduction and early development in mallards.

Upon finding a suitable nesting site, typically a shal-low crevice in the ground, the mallard hen begins to lay her eggs, at the rate of one egg per day (Miller and Gottlieb 1978). The average clutch size is eight to ten, and after the last egg is laid the hen begins incubation, a process that lasts approximately 26 days. Encouraged by the warmth of the mother’s body, the embryo inside each egg begins to develop. Two to three days before hatching, each embryo moves its head into the air space within its egg and begins to vocalize; these vocalizations are called contentment calls. About 24 hours later, the embryos pip the outer shell and then take another day to break through the rest of the shell and hatch. Most of the ducklings in a clutch will hatch within an inter-val of ten hours. The hen broods her young for a day and then leaves the nest and emits calls to encourage the ducklings to follow. Although she vocalizes during incu-bation and brooding, the frequency increases dramati-cally at the time of the nest exodus. Prompted by their mother’s assembly calls, the young leave the nest and follow her to a nearby pond or lake, where they will pad-dle behind her.

Observations such as these stimulate many ques-tions. What characteristics of the mother form the basis for the ducklings’ attachment? Do the ducklings imprint on the mother’s call, physical appearance, or some com-bination of the two? What role might siblings play in the development of the following response? Finally, is there a sensitive period during which exposure to cer-tain cues must occur for the normal development of fil-ial behavior?

Many of the answers to these questions came from the laboratory of Gilbert Gottlieb, a pioneer in behav-ioral development who passed away in 2006. For several decades, Gottlieb and co-workers examined the devel-opment of the following response in Peking ducks, a domestic form of the mallard (despite their domestica-tion, Peking ducks are quite similar to their wild coun-terparts in their behavior). Here we consider some of the work of Gottlieb and his colleagues.

In one experiment with ducklings that had never had contact with the mother, Gottlieb (1978) examined (1) the relative importance of the hen’s auditory and visual

cues in the development of the following response and (2) whether the parental call of a duckling’s own species would be more effective than that of other species in inducing and maintaining attachment behavior. As part of the study, 224 eggs were hatched in an incubator; thus, the ducklings never came in contact with their mothers.

The ducklings were divided into four groups and tested for their following response. In all four groups, the duck-lings were tested with a stuffed replica of a Peking hen as it moved about a circular runway. Individuals in one of the groups, however, were tested with a silent hen, whereas individuals in the other three groups were tested with hens that emitted assembly calls through a speaker concealed on their undersides. Of the ducklings that heard assembly calls, one group was exposed to mallard calls (Peking calls), one group to wood duck calls, and one group to domestic chicken calls. Each duckling was given a 20-minute test to determine whether it would follow the stuffed model around the circular arena.

The results are presented in Figure 8.11. As you can see, the auditory stimulus of the maternal call is impor-tant in filial imprinting: all conditions with calls were much more effective than no call at all. Furthermore, even though the ducklings had never before heard the maternal call of their species, they responded selectively to it. The maternal call of the mallard was far more effec-tive than that of the wood duck or chicken in inducing following by the ducklings.

Percentage following

100

50

0 Mallard Wood duck Chicken Silence

Experimental condition

FIGURE8.11 A stuffed Peking hen emitting mallard calls was more effective in eliciting the following response in incubator-reared Peking ducklings than a hen emitting either wood duck or chicken calls (Peking ducks are a domestic form of the mallard duck). All hens with calls were more effective than a silent hen. Thus, auditory cues from the mother are important in controlling the early behavior of ducklings, and ducklings respond selectively to the call of their own species without previous exposure to it. (Drawn from the data of Gottlieb 1965.)

In a second experiment, incubator-reared ducklings were given a choice of following either a stuffed Peking hen that was emitting mallard calls or a stuffed Peking hen that was emitting chicken calls. When placed in this simultaneous choice situation approximately one day after hatching, the majority of ducklings (76%) followed the model that was emitting the mallard call.

Taken together, these experiments demonstrate that auditory stimuli from the mother are an important influence on the behavior of newly hatched ducklings.

Furthermore, ducklings respond selectively to the maternal assembly call of their own species without any previous exposure to it (remember that all ducklings were reared in incubators and therefore had no contact with hens). This preferential response by the ducklings to the assembly call of their species is an example of the predisposition described earlier. Recall that young pre-cocial birds may develop a preference for stimuli from conspecifics without prior exposure to the particular stimuli.

These findings do not, however, suggest that expe-rience is unimportant in the development of a prefer-ence for the assembly call. Experiprefer-ence, as it turns out, is critical, but it occurs prenatally (before hatching). For Peking ducklings to exhibit a preference for the mallard hen’s call, they must hear their own contentment calls or those of their siblings before hatching (Gottlieb 1978). If ducklings are reared in isolation (and therefore are not exposed to the calls of their siblings) and made mute just before they begin to vocalize within the egg (and therefore are not exposed to their own calls), they no longer display their highly selective response to the maternal call of their species. When these ducklings without normal embryonic auditory experience are placed in a test apparatus equidistant between two speakers, one speaker emitting a mallard’s maternal call and the other a chicken’s maternal call, they choose the latter almost as often as they choose the former 48 hours after hatching. In contrast, ducklings with normal

embryonic auditory experience always choose the mal-lard’s call over the chicken’s (Table 8.1). Thus, auditory experience before hatching is important to the devel-opment of the following response in mallard ducklings because it induces a predisposition to approach the mal-lard assembly call.

Is there a sensitive period during which exposure to contentment calls must occur for ducklings to exhibit a preference for the call of the mallard hen? If ducklings heard contentment calls after hatching, would they dis-play the normal preference for mallard calls? Gottlieb (1985) set out to answer these questions. He began by raising ducklings in isolation and making them mute before they began to vocalize within the egg (again, these manipulations ensure that the ducklings are not exposed to their own calls or the calls of their siblings). One group was exposed to contentment calls during the embryonic period (approximately 24 hours prior to hatching), and another group was exposed to content-ment calls during the postnatal period (approximately 24 hours after hatching). Ducklings in each group were then tested for their preference for the mallard hen’s call. This time, however, they were given the choice of approach-ing a speaker that emitted normal calls of a mallard hen or a speaker that emitted artificially slowed calls of a mal-lard hen. As shown in Table 8.2, ducklings must be exposed to contentment calls before hatching if they are to show a preference for the normal call; exposure after hatching is ineffective in producing the preference for the normal call of their species. Here, then, we have an example of a sensitive period occurring during embry-onic development.

What role, if any, might visual stimuli play in the development of the following response? Several experi-ments have shown that two conditions must be simulta-neously met if visual imprinting on a mallard hen is to occur in the ducklings. The ducklings must be reared with other ducklings and allowed to actively follow a mallard hen, or a model, if they are to prefer the

appear-T

ABLE

8.1

The Effects of Embryonic Auditory Experience on Call Preferences of Peking Ducklings 48 Hours after Hatching

Preference

N Mallard call Chicken call Both

Vocal-communal 24 24 0 0

Mute-isolated

First experiment 22 12 9 1

Replication 21 14 6 1

Total 43 26 15 2

Ducklings raised in the vocal-communal group could hear themselves and the calls of siblings prior to hatching; mute-isolated ducklings had no such auditory experience. N⫽ number of ducklings that responded to calls.

Source: Data from Gottlieb (1978).

ance of a hen of their own species to that of a hen of another species at later testing (e.g., Dyer et al. 1989;

Lickliter and Gottlieb 1988). Ducklings that are reared in isolation and given passive exposure to a stuffed mal-lard hen (i.e., housed with a stationary model) do not develop a preference for the mallard hen. These results suggest that under natural conditions, ducklings learn the visual characteristics of their mother after leaving the nest and following her around.

We see, then, that both auditory and visual stimuli are important in development of the following response.

Auditory stimulation from the mother appears to be largely responsible for prompting the ducklings to leave the nest and for influencing their earliest following behavior. However, the hen’s appearance becomes important after the nest exodus.

The importance in filial imprinting of auditory cues, visual cues, and active following was well summarized by Lorenz (1952, pp. 42–43). In an experiment with Peking ducklings, he found himself in a rather embarrassing position for one destined to become a Nobel Laureate.

In his words,

The freshly hatched ducklings have an inborn reaction to the call-note, but not to the optical picture of the mother. Anything that emits the right quack note will be considered as mother, whether it is a fat white Peking duck or a still fatter man. However, the substi-tuted object must not exceed a certain height. At the beginning of these experiments, I had sat myself down in the grass amongst the ducklings and, in order to make them follow me, had dragged myself, sitting, away from them. So it came about, on a certain Whit-Sunday, that, in company with my ducklings, I was wandering about, squatting and quacking, in a May-green meadow at the upper part of our garden. I was congratulating myself on the obedience and exactitude with which my ducklings came waddling after me, when I suddenly looked up and saw the garden fence framed by a row of dead-white faces: a group of tourists was standing at the fence and staring horrified in my direction. Forgivable! For all they could see was a big man with a beard dragging himself, crouching,

round the meadow, in figures of eight, glancing con-stantly over his shoulder and quacking—but the duck-lings, the all-revealing and all-explaining ducklings were hidden in the tall spring grass from the view of the astonished crowd!

To summarize, the experiments of Gilbert Gottlieb and co-workers have demonstrated that the following response in Peking ducklings results from a complex interaction of auditory, visual, and social stimuli pro-vided by the hen and siblings. Several important gen-eralizations about early behavioral development have arisen from their work. First, we can no longer think of experience as occurring only after birth or hatching;

embryonic experience can also influence behavior. In the case of Peking ducklings, listening to the content-ment calls of siblings before hatching is critical to devel-opment of their preference for the maternal call of their own species after hatching. Second, the experiments with ducklings demonstrate that a variety of stimuli may be involved in developing a single pattern of behavior and that the relative importance of different stimuli may change as the young animal matures. Although the fol-lowing behavior of ducklings soon after hatching is influenced largely by auditory cues from their mother, only a few days later visual stimuli (in combination with auditory stimuli) become important in the following response. The relative priorities of different cues match the timing for development of the auditory and visual systems; in ducklings, as in all birds, the auditory sys-tem develops before the visual syssys-tem (Gottlieb 1968).

These results emphasize the close interaction between physical maturation and experience in early behavioral development. Finally, the study of filial imprinting in Peking ducklings illustrates that we must be open-minded when trying to sort out just which experiences affect a given behavior. Who would have thought that listening to siblings before hatching or interacting with siblings after hatching would be critical in the develop-ment of the ducklings’ attachdevelop-ment to their mother? We now know that such nonobvious experiential factors are indeed essential to the development of following behav-ior in this species.

T

ABLE

8.2

Effects on Preferences of Mute-Isolated Ducklings of Embryonic Versus Postnatal Exposure to Contentment Calls

Preference Time of exposure to

contentment calls N Normal mallard Slowed mallard Both

Embryonic 32 21 8 3

Postnatal 37 14 20 3

Source: Data from Gottlieb (1985).