The development of postnatal turning bias is influenced by prenatal visual experience in domestic chicks (Gallus gallus).
Rogers and her colleagues (Rogers, 1982; Rogers & Bolden, 1991; Rogers & Workman, 1989) have demonstrated that the direction of lateralization in the domestic chick forebrain is determined, at least in part, by the asymmetrical prenatal visual experience of the developing embryo (see Rogers, 1991, for review). At the onset of the lengthy hatching process, the chick embryo is oriented in the egg such that its left eye is blocked by the body and yolk sac, while the right eye is exposed to light entering through the shell. Furthermore, this embryonic orientation occurs at a developmental stage in which the central visual connections are becoming functional and when light stimulation can elicit motor responses (Rogers, 1991). Rogers has argued that the differential prenatal visual experience that results from the asymmetrical orientation of the embryo just prior to hatching serves to facilitate the development of the left hemisphere in advance of the right.
Turning Biases and Spatial Orientation
Rotatory or turning biases are a variety of motor asymmetry in which an animal turns all or part of its body toward one side (left or right) in responding to sensory stimuli. Such biases have been studied in several species, rats (Denenberg, Garbanati, Sherman, Yutzey, & Kaplan, 1978; Glick, 1985), primates (Warren, 1977; Westergaard & Suomi, 1996), and humans (Bradshaw & Bradshaw, 1988; Melekian, 1981). Turning biases are significant because they appear to be evolutionarily old and many motor behaviors have become associated with such behavioral asymmetries (Gospe, Mora, & Glick, 1990; Schone, 1984). For example, lateralized nervous system activity may trigger turning, and conversely, turning may induce other asymmetric activities.
Although extensively studied in mammalian species, turning and rotational biases have been given less of an empirical focus in birds. In the following experiment, we examined the role that prenatal sensory experience plays in the development of turning bias in domestic chicks. Because visual experience has been demonstrated as a powerful prenatal lateralizing influence in other studies of precocial birds, we hypothesized that prenatal visual experience would also prove to be a significant influence on postnatal motor asymmetry in domestic chicks.
Maternally naive, incubator-reared domestic chicks (Gallus gallus) served as subjects. Fertile, unincubated eggs were received weekly from a commercial supplier and set in a Hovi-bator portable incubator, maintained at 37.5 [degrees] C and 80-85% humidity. Eggs were incubated until Day 20 in relative darkness. Incidental exposure to light may have occurred when water was added to the incubator, but for a very brief period. Plastic viewing holes were blocked by thick black cardboard. After 20 days of incubation, the eggs were transferred to a hatching incubator. The possible influence of between-hatch variation in behavior was controlled by drawing subjects for each experiment from at least two different egg batches.
Following hatching, each chick was labeled with a small, water-soluble colored dot on the top of its head. Chicks were then placed in large plastic brooders which contained 8-12 same-aged chicks. Brooder temperatures were maintained at approximately 37 C. Group size was chosen to mimic naturally occurring brood conditions. Food and water were continuously available to subjects throughout the experiments.
The testing apparatus consisted of a T maze (20 cm high x 6 cm wide; stem = 13 cm long; T arms - 14 cm long) constructed within a large plastic brooder (identical to those used for rearing chicks). This arrangement was used to maintain consistency between rearing and testing conditions, and reducing any nonobvious effects between rearing and testing conditions (see Casey & Lickliter, 1996, for discussion of similar effects). Temperature in the testing apparatus was maintained at approximately 37 [degrees] C. A small tape player was located immediately behind the T maze equidistant from opposite ends. . The auditory stimuli consisted of a continuously looped recording of a domestic chicken maternal call.
Individual turning bias indices were computed using a typical laterality formula (see Corballis, 1991; Denenberg, 1981). The formula produces a quantitative index for the direction of turning bias: (R - L)/(R + L). The numerator is the number of right-side responses (by an individual chick at each of the 12 trials) minus the number of left-side responses. The denominator is the total number of responses made by that chick (i.e., 12). A positive score indicates a right-side bias, a negative score reflects a left bias, with zero indicating no lateral bias. Thus, individual level turning biases are defined as a general propensity to make left or right turns.
Subjects were individually placed in the stem of the T maze. A lab assistant (who was unaware of the subject's experimental condition) simultaneously began the domestic chicken maternal assembly call tape and recorded the side (right or left) that was first approached (i.e., turning side bias) by the chick in the T maze. Testing began at least 48 hours following hatch. Each chick was tested 12 times across a 96-hr period. These times allowed for at least three testing trials per day with at least 4 hours between each session. Multiple testing times were necessary to establish the presence or absence of individual lateralization.
Subjects were incubated under intermittent light conditions as might be expected of quail hatched in the wild. Incubators were kept in a darkened room as described above. During the second half of the 20th day of incubation, the shell and inner-shell membrane over the air space of the egg of each subject were removed and the embryo's head gently pulled out of the shell. The embryo's bill typically penetrates the air space early on Day 20 of incubation. The embryo begins to respire and vocalize following penetration into the air space (Vince, 1972). Thus, exposing the embryo's head at this time (the embryo's body remains in the shell) does not interfere with the final stages of incubation (Heaton & Galleher, 1981; Lickliter, 1990).
Right- and left-eye systems were occluded with water-resistant white surgical tape. A piece of tape 1.5 cm by 1.5 cm was cut .75 cm down the middle. The tape was folded over to form a cone-shaped patch. This patch was applied over the eye (right or left), thus dramatically attenuating visual stimulation to the contralateral hemisphere (see Zappia & Rogers, 1983, 1987, for similar procedures). Following removal of part of the shell and eye occlusion, opened eggs were placed in a Hovi-bator portable incubator for the last 24 hr of incubation. This incubator was outfitted with a clear Plexiglas top, allowing both observation and stimulation of the embryos. Consistent temperature and humidity levels were maintained as during control incubation, therefore experimental embryos and control embryos did not differ in their developmental age at hatch.
Group 1 consisted of 30 subjects that had both eye systems (RES and LES) exposed to enhanced visual stimulation. Group 2 consisted of 30 subjects that had their right-eye system (RES) patched and their left-eye system (LES) given enhanced visual stimulation. Group 3 consisted of 30 control subjects with their left-eye system (LES) patched and their right-eye system (RES) given enhanced visual stimulation.
Embryos in Groups 1, 2, and 3 were exposed to the light of a 60-W bulb for 24 hr prior to hatching. Particular care was taken to ensure that the presence of the light did not alter the ambient air temperature or relative humidity within the incubator. Following hatching, chicks were placed in plastic brooders with same-aged conspecifics to mimic naturalistic brooding conditions.
As a general control condition for the experiment, 30 maternally naive domestic chicks were tested following procedures detailed above. Subjects demonstrated individual and group level turning biases. Overall 27 out of 30 subjects were left-side biased (90%), 3 subjects were right-side biased (10%), and no subjects were found to be unbiased (see Table 1).
Chicks in Group 1 had both left and right eyes exposed to enhanced visual stimulation. Thirteen subjects were left-side biased (43%), 14 subjects were right-side biased (46%), and 3 subjects were unbiased (see Table 1). A chi-square test revealed that side-bias distributions differed significantly from those found in unmanipulated chicks ([[Chi].sup.2] = 47.59, p [less than] .05).
Table 1 Effects of Differential Prenatal Visual Experience on Development of Postnatal Turning Bias Turning Bias Subject Group N Right Bias Left Bias No Bias Control 30 3 27 (NS) Group 1 30 14 13 3 (Both ES stim) Group 2 30 16 14 0 (LES stim) Group 3 30 3 26 1 (RES stim) Note. NS = no enhanced stim; ES: eye system; LES stim = left-eye system stimulated; RES = stim right-eye system stimulated.
Chicks in Group 2 had their right-eye systems (RES) occluded, and their left-eye system (LES) exposed to enhanced visual stimulation. Fourteen subjects were left-side biased (46%), 16 subjects were right-side biased (53%), and no subjects were unbiased (see Table 1). A chi-square test indicated that these side-bias distributions differed significantly from expected distributions found in unmanipulated subjects ([[Chi].sup.2] = 62.59, p [less than] .05).
Chicks in Group 3 had their left-eye system occluded, and their right-eye system exposed to enhanced visual stimulation. Overall 26 of 30 subjects demonstrated a left-side turning bias (86%), 3 subjects were right-side biased (10%), and 1 subject was unbiased (see Table 1). Side-bias distributions did not differ significantly from expected distributions found in unmanipulated chicks (p [greater than] .05). Exposing the chick's RES to enhanced prenatal visual stimulation (the species typical developmental pattern) appeared to induce a significant group level of left-side turning bias.
The developmental processes that lead to turning biases in spatial orientation have been examined in a variety of mammalian species (Denenberg, 1977; Ridgeway, 1986). However, such developmental influences have not been investigated to any extent in birds. This study demonstrated a left-side population turning bias (in a standard T maze) in domestic chicks (Gallus gallus). Control tests revealed a left-side turning bias in 90% of subjects. This finding alone is striking in that such a large group bias is highly unusual in nonmammalian species. It is only in humans (the other bipedal species) that such large percentages are typically found.
Chicks in the experimental conditions were exposed to one of three prenatal conditions: both eye systems exposed to enhanced visual experience, right-eye system exposed/left-eye system occluded, or left-eye system exposed/right-eye system occluded. Only those subjects that received unilateral right-eye visual stimulation prenatally demonstrated a population level left-side turning bias similar to that found in controls. These results suggest that unilateral prenatal visual experience to the right eye/left hemisphere is a significant contributor/facilitator to the lateralization process in domestic chicks. Chick embryos that received unilateral left-eye visual stimulation or bilateral visual stimulation demonstrated individual lateralization, but not population lateralization (e.g., more than 50% of subjects being left or right biased.
This further suggests that the development of left-side turning bias is not predetermined in some way (genetic, for example), as might be concluded from such a large population bias in control subjects, but the result of a highly structured, almost invariant, environmental influence. To successfully hatch, the posture of the chick embryo must be oriented toward the top of the egg with the right side facing outward, thus providing a greater degree of mobility to the right side of the body (Oppenheim, 1972). This, in turn, provides more sensory and motor experience to the right side of the body, which appears to facilitate the development of hemispheric lateralization and related behavioral asymmetry (see Denenberg, 1981, for a similar argument in mammalian species).
In addition to the conclusion that postnatal turning bias is mediated by unilateral prenatal visual experience to the right-eye system, it may be possible that this early prenatal sensory experience, when provided in a species atypical way (visual experience to the left-eye system), actually overrides or suppresses the development of left hemispheric structures. Thus providing a developmental edge to the right hemisphere instead of the left as is usually the case. In any case, these findings parallel other lateralization work in domestic chicks (see Rogers, 1991, for an excellent review). Prenatal visual stimulation appears to synchronize the direction of population level laterality, if not specifically inducing individual lateralization for a wide range of postnatal sensory, perceptual, and motor abilities (Rogers, 1982; Zappia & Rogers, 1983).
Kuo (1967) argued that every behavior is a functional product of the dynamic interrelationship of five groups of determining factors (biochemical, morphological, developmental history, immediate stimulus array, and environmental context). This system of transacting constraints and fluctuating degrees of freedom can be seen in the developmental relationship between prenatal sensori-motor experience, hemispheric specialization, and behavioral asymmetries. Clearly, prenatal organismic factors (the orientation of the embryo prior to hatching) and environmental factors (differential exposure to visual experience) interact to produce a basic lateralized postnatal behavior. This experiment has demonstrated that visual experience is a critical factor in the development of turning bias in domestic chicks. Thus, prenatal sensory experience is not only a significant influence on the lateralization process and the development of perceptual asymmetries, but of motor asymmetries as well. Future work must explore in greater detail any effects on the neural substrate in the right and left hemispheres of the domestic chick that contribute to motor asymmetries such as postnatal turning bias.
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|Author:||Casey, Michael B.; Karpinski, Stephanie|
|Publication:||The Psychological Record|
|Date:||Jan 1, 1999|
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