Specific postnatal auditory stimulation interferes with species-typical visual responsiveness in...

Specific Postnatal Auditory Siirnulation Interferes with Species-Typical Visual Responsiveness in Bobwhite Quail Chicks THOMAS MCBRIDE ROBERT LICKLITER Department of Psychology Virginia Pofytechnic Institute and State University Blacksburg, Virginia

The effects that a manipulation of sensory experience may have on perceptual development are likely to depend on a number of factors, including the amount and the type of stimulation provided. To examine the relative influence of these stimulation factors on early perceptual organization, this study exposed bobwhite quail hatchlings to augmented amounts of bobwhite chick distress calls, bobwhite chick contentment calls, domestic chicken distress calls, or no additional auditory stimulation during the first 72 hr following hatching. Results showed that bobwhite hatchlings exposed to bobwhite chick distress calls do not exhibit species- typical visual responsiveness to maternal cues. In contrast, bobwhite hatchlings exposed to bobwhite chick contentment calls, domestic chicken hatchling distress calls, or no agumented auditory stimulation exhibited species-typical auditory and visual responsiveness to maternal cues. These results demonstrate intermodal effects of postnatal sensory stimulation and suggest that specific types of postnatal auditory stimulation, rather than simply increased amount of stimulation, are necessary to interfere with species-typical intersensory functioning. 0 1994 John Wiley & Sons, Inc.

A number of recent studies have shown that manipulating the early sensory experience of precocial birds can change responsiveness to species-specific perceptual cues (see Lickliter, 1993 for a review). These findings concerned with the dynamics of early perceptual organization raise the interesting question of under what conditions specific manipulations of early sensory experience serve to either facilitate or interfere with the usual course of perinatal perceptual development. Specifically, it is not clear why some manipulations of sensory experience result in the facilitation of perceptual functioning, while other sensory manipulations appear to impede or interfere with early

Reprint requests should be sent to Robert Lickliter, Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061-0436, U.S.A.

Received for publication 15 July 1993 Revised for publication 5 November 1993 Accepted for publication 15 November 1993

Deueloprnental Psychobiology 27(3): 169-183 (1994) 0 1994 by John Wiley & Sons, Inc. CCC 0012-16301941030169-1 5

170 MCBRIDE AND LICKLITER

perceptual abilities. For example, unusually early (prenatal) visual experience has been found to accelerate species-typical visual functioning in bobwhite quail chicks (Lickliter, 1990a). Chicks exposed to patterned light as embryos responded to species-specific maternal visual cues at an earlier age than unmanipulated control chicks. On the other hand, unusually early visual experience has also been found to interfere with species- typical auditory responsiveness in bobwhite chicks (Lickliter, 1990a, 1990b). Whereas normally rearcd chicks show a significant preference for the bobwhite maternal call over a nonconspecific call at both 24 hr and 48 hr following hatching (Lickliter & Virkar, 1989), chicks exposed to patterned light as embryos do not exhibit a preference for the bobwhite maternal call at either 24 hr or 48 hr following hatching.

It seems likely that whether a particular manipulation of sensory experience serves to facilitate or interfere with perceptual development will depend on several factors. One possible factor affecting the impact of altered sensory stimulation history is the age of the infant at the time of the experimental manipulation. For example, the previously mentioned studies all manipulated aspects of prenatal sensory experience. The manipulation of prenatal stimulation history may be more likely to affect the dynamics of subsequcnt sensory system functioning than similar postnatal manipulations, in that the sensory systems are still undergoing rapid development during the prenatal period (Gottlieb, 1971; but see Banker & Lickliter, 1993 for an alternative view).

A second factor associated with the influence of sensory experience may be the amount of stimulation that the developing organism encounters. For example, based on their findings from enhanced vestibular stimulation in duck embryos, Radell and Gottlieb (1992) proposed that the amount of sensory experience normally encountered by a developing organism can be seen as optimal for its species-typical perceptual development. They argue that any substantial and enduring deviation from the normal amount of sensory experience typically encountered by the developing individual should lead to functional deficits in perceptual capacity. In contrast, exposure to species- typical or only slightly augmented levels of sensory experience should result in typical or even facilitated intersensory development, which may explain the accelerated pattern of visual responsiveness seen in bobwhite quail chicks exposed to augmented prenatal auditory experience (Lickliter & Stoumbos, 1991).

In addition to amount of stimulation, a third possible factor underlying the effects of sensory stimulation history may be the specific type of stimulation to which the developing organism is exposed. For example, Lickliter and Stoumbos (1991) exposed bobwhite quail embryos to increased amounts of their own normally occurring embryonic vocalizations during the days immediately prior to hatching. When tested postna- tally, these birds showed an accelerated pattern of responsiveness to species-specific maternal visual cues. In contrast, bobwhite quail embryos exposed to bobwhite embryonic vocalizations with a faster repetition rate than normal did not show an accelerated pattern of postnatal visual responsiveness (Lickliter & Stoumbos, 1991), suggesting that the type of stimulation provided is an important factor in how sensory experience affects subsequent perceptual abilities.

In sum, the effect that a manipulation of sensory experience may have on perceptual development is likely to depend on a number of factors, including the timing of the manipulation, the amount of stimulation, and the type of sensory stimulation provided. As a first step in examining the relative influence of these factors on early perceptual organization, this study assessed the effects of different types of postnatal auditory stimulation on the development of species-specific auditory and visual responsiveness in bobwhite quail chicks. Specifically, group-reared bobwhite quail hatchlings were

AUDITORY STIMULATION AND VISUAL RESPONSIVENESS 17 1

exposed to augmented amounts of either bobwhite hatchling distress calls, bobwhite hatchling contentment calls, or domestic chicken hatchling distress calls during the first 3 days following hatching. It is important to note that the term “augmented” is used here to refer to auditory stimulation made available in addition to subjects’ own self- produced auditory stimulation during the posthatch period.

Group-reared bobwhite quail chicks’ vocalizations during the posthatch period typically consist of contentment calls (McBride & Lickliter, 1993; see Stoumbos & Lickliter, 1990 for acoustical details); in contrast, distress calls (see Stoumbos & Lickliter, 1990 for acoustical details) are rarely observed in brood-reared chicks during the days immediately following hatching (McBride & Lickliter, 1993). Thus, one type of auditory stimulation employed in the present study (the contentment call) is normally present in the posthatch environment of young hatchlings, whereas the other types of auditory stimulation presented in this study (the bobwhite hatchling distress call and the chicken hatchling distress call) are typically infrequent or absent in the chick’s posthatch environment.

If substantial increases in amounr of auditory stimulation present in the postnatal environment is sufficient to result in functional deficits in species-typical auditory or visual responsiveness, then increased exposure to either distress calls or contentment calls should interfere with chicks’ subsequent perceptual abilities. On the other hand, if type of stimulation is the more important factor in determining subsequent effects on perceptual responsiveness, then exposure to either distress calls or contentment calls should differentially impact chicks’ subsequent perceptual responsiveness. The present study was designed to assess these two possibilities.

General Methods

Subjects Maternally naive, incubator-reared bobwhite quail chicks (Cofinus uivginianus)

served as subjects. Fertile, unincubated eggs were received weekly from a commercial supplier and set in a Petersime Model I incubator, maintained at 37.5”C and 90-95% humidity. After 20 days of incubation, the eggs were transferred to a hatching tray located in the bottom of the incubator. Only those birds that hatched between the second half of Day 22 and the first half of Day 23 of incubation were used as subjects (By convention, Day 23 of incubation begins at Day 23, 0 hr and ends at Day 23, 23 hr.) This constraint controlled for the possible effects of variations in developmental age. The possible influence of between-hatch variation in behavior was controlled by drawing subjects for each experiment from at least three different batches of eggs.

Following hatching, chicks were placed in large plastic tubs (45 x 25 x 15 em) which contained 12-18 same-aged chicks. This group size was chosen to mimic naturally occurring brood conditions (Stokes, 1967). The room in which the hatchlings were kept was illuminated by a 100-W brooder lamp suspended above the plastic rearing tubs, which maintained an ambient air temperature of approximately 30°C. Food and water were continuously available throughout the course of the experiments.

Testing Apparatus and Stimuli The testing apparatus was located in a sound-attenuated room and consisted of a

large circular arena, 160 cm in diameter, surrounded by a black curtain that shielded the observer from the subject’s view. The walls of the apparatus were lined with foam


to attenuate echoes and the floor was painted flat black. Two rectangular approach areas (32 x 15 cm) were delineated on opposite sides of the arena by green lines painted on the floor.

The auditory stimuli used in this study were recordings of a bobwhite quail maternal call (see Heaton, Miller, & Goodwin, 1978 for acoustical details) and a domestic chicken (Gallus domesticus) maternal call (see Gottlieb, 1971 for acoustical details). The auditory stimulus tapes were looped to repeat continuously during the 5-min test trial. A midrange dome radiator speaker was positioned behind the curtain of the arena in each of the approach areas, equidistant from the point at which each subject was placed in the apparatus. These speakers allowed the simultaneous presentation of the species-typical and species-atypical maternal calls during the test trial. Each speaker was connected to a Tascam model 122-B cassette tape recorder located at a control table. The observer was seated at this table and observed each subject’s activity through a large mirror positioned above the arena. A system of hand-operated stopwatches was used to score the latency and duration of response, as described below. Two taxidermically prepared natural models of quail hens served as the visual stimuli in the simultaneous choice tests. One model was an adult bobwhite (Colinus uirginianus) hen, the other an adult scaled quail (Callipepla squamata) hen, a species whose habitat range overlaps that of the bobwhite quail (Johnsgrad, 1973; for a photograph of the two hens, see Lickliter & Virkar, 1989). Previous research has shown that both forms of auditory stimuli (the bobwhite maternal call and the chicken maternal call) and visual stimuli (bobwhite hen replica and scaled hen replica) employed are adequate, at least under some experimental conditions, to elicit preferential responsiveness on the part of bobwhite chicks (Lickliter, in press; Lickliter & Virkar, 1989). The testing room was maintained at approximately 26°C throughout the study.

Testing One simultaneous choice test, 5 min in length, was given to each chick at 72 h r

( + 3 hr) following hatching. The birds were tested for their preference between either auditory or auditoryhisual stimuli presented on either side of the arena. Presentation of the stimuli was counterbalanced across subjects to prevent a possible side bias from affecting the results. In the test trials, each quail hatchling was placed singly in the test apparatus, equidistant from the two approach areas. The latency and duration of a subject’s response to the test stimuli was scored as follows: As the bird entered each approach area, its choice, the latency (amount of time elapsed in seconds from the onset of the trial), and duration (the cumulative amount of time in seconds the bird remained in the approach area) of response was recorded. When over the course of the 5-min test a chick stayed in one approach area for more than twice the time it spent in the opposing area, a preference was registered. Occasionally a bird entered both approach areas during a test without showing a preference for either one. This behavior was scored as “Both” in the tables showing the test results. If a subject did not enter either approach area, it was considered a “nonresponder” and received a score of 300 s for latency (the length of the trial) and 0 s for duration for both test stimuli.

Data Analysis Before performing any statistical analyses, testing duration scores of less than

10 s were replaced with a score of 0 to avoid scoring accidental responses as subjects moved about the area. The corresponding latency score were replaced with a score of

AUDITORY STIMULATION AND VISUAL RESPONSIVENESS 173

300 s (the length of the testing trial). The primary data of interest in this study were measures of preference for the auditory and visual stimuli presented during the trials. Three such measures of preference were analyzed: (a) differences in the latency and (b) duration of time spent in proximity to each stimulus by a subject in a group was evaluated by the Wilcoxon matched-pairs signed-ranks test, and (c) individual preference, assigned to any subject that stayed in proximity to one stimulus for more than twice as long as the other, was evaluated by the chi-square test. Significance levels of p < .05 were used to evaluate results.

Experiment 1: Auditory and Visual Responsiveness of Unmanipulated Chicks As a first step in examining the effects of augmented postnatal auditory experience

on subsequent perceptual functioning, the auditory and visually based responsiveness of group-reared bobwhite quail chicks that were not exposed to any additional postnatal auditory stimulation were assessed. Previous research with bobwhite quail chicks has demonstrated a hierarchy in the functional priority of the auditory and visual systems in the days immediately following hatching (Lickliter, in press; Lickliter & Virkar, 1989). At 24 and 48 hr of age, species identification is dependent on the auditory component of maternal stimulation. In other words, chicks require only the bobwhite maternal call to direct their filial behavior during the first 2 days following hatching. However, by 72 hr following hatching combined maternal auditory and visual stimulation (i.e., the bobwhite maternal call and the bobwhite hen model) is necessary to success- fully direct chicks’ social preferences. In addition, hatchlings show a significant visual preference for a bobwhite hen model over a scaled quail hen model when both are emitting the same bobwhite maternal call by 72 hr following hatching (but not at earlier ages). It is important to note that the static visual cues provided by the hen modeIs alone are not sufficient to elicit preferential responsiveness at any ages tested. Rather, maternal visual cues must be presented with the maternal call to be effective in directing social preferences (Lickliter, in press; Lickliter & Virkar, 1989).

In order to replicate these earlier findings and to provide the necessary controls for the subsequent experiments of this study, socially reared hatchlings’ responsiveness to both maternal auditory cues and maternal visual cues were assessed at 72 hr following hatching. Based on the results of previous studies, the birds were expected to demonstrate a significant preference for maternal visual cues (when presented with the maternal call) at this age, but to no longer prefer maternal auditory cues when presented alone (without maternal visual cues).

Method

Forty-one bobwhite quail chicks, drawn from three separate hatches, served as subjects. Chicks were divided into two groups for testing purposes. Nineteen chicks were individually tested in a simultaneous choice test between a bobwhite maternal call and a chicken maternal call at 72 hr following hatching (auditory group). Twenty- two subjects were individually tested in a simultaneous choice test between a bobwhite maternal call paired with a stuffed bobwhite hen replica and the same bobwhite maternal call paired with a stuffed scaled quail hen replica(visua1 group). Since both the bobwhite hen and the scaled hen were emitting the same auditory cue (i.e., the bobwhite maternal call), subjects in this test situation were required to base their preferential responding


Table 1 Preference of Chicks in Simultaneous Auditory Choice Tests ~

Preference

Bobwhite Chicken 1% Maternal Maternal

n responding Call Call Both

Control 19 6 6 0 0 Bobwhite Contentment Calls 25 8 7 1 0 Bobwhite Distress Calls 25 10 9 1 0 Chicken Hatchling Distress Calls 18 7 7 0 0

on the avai,,,,: visual cues provided by the hens. Choice, latency, anc -xation were scored as described in the General Methods section.

Results and Discussion The results of testing are shown in Tables 1 and 2. As expected, chicks that were

tested at 72 hr following hatching in the auditory test between the bobwhite maternal call and the chicken maternal call did not show a consistent pattern of responsiveness to the bobwhite maternal call (Table 1). Only 6 of 19 birds tested (31%) responded in the simultaneous choice test. Ofthe 6 chicks that did respond, all preferred the bobwhite maternal call over the chicken maternal call. This finding parallels the results of previous studies (Banker & Lickliter, 1993; Lickliter & Virkar, 1989), which found that bobwhite chicks show a sharp decline in auditory responsiveness to maternal auditory cues (when presented alone) by 72 hr following hatching.

Chicks that were tested in the simultaneous choice test between a bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paircd

Table 2 Preference of Chicks in Simultaneous Auditory-Visual Choice Tests

Preference

Bobwhite Maternal Bobwhite Maternal n Call and Bobwhite Call and Scaled

n responding Hen Hen Both

Control 22 21 13" Bobwhite Contentment Calls 25 21 12* Bobwhite Distress Calls 25 20 1 Chicken Hatchling Distress Calls 25 17 15*

* p < .05 (chi-square test).


with a stuffed scaled quail hen displayed a significant preference for the bobwhite maternal call paired with the bobwhite hen at 72 hr following hatching, p < .05, Table 2. This result was further supported by analysis of the latency and duration scores: There were significantly shorter latencies and longer duration scores in the subjects’ responses to the bobwhite maternal call paired with the model of the bobwhite hen, Wilcoxon signed-ranks test, p < .001 in both cases. These results parallel the results of previous studies (Lickliter & Virkar, 1989; McBride & Lickliter, 1993) demonstrating naive chicks’ abilities to utilize maternal visual cues by 72 hr following hatching and provides the necessary control group for the subsequent experiments of this study.

Experiment 2: Auditory and Visual Responsiveness of Chicks Exposed to Bobwhite Contentment Calls In order to begin assessing whether augmented postnatal auditory stimulation facili-

tates or interferes with bobwhite chicks’ species-typical perceptual abilities, chicks in this experiment were exposed to bobwhite hatchling contentment calls during the first 3 days following hatching. If augmented amounts of postnatal auditory stimulation do serve to alter chicks’ responsiveness to species-specific auditory or visual cues, then chicks exposed to augmented amounts of bobwhite hatchling contentment calls should respond to maternal auditory and visual cues differently than the control chicks in the previous experiment.

Method Forty-six bobwhite quail chicks, drawn from three separate hatches, served as

subjects. Following hatching, all chicks were placed in social groups containing 12-18 same-aged chicks and were exposed to 45 min of recorded bobwhite hatchling contentment calls (see Stoumbos & Lickliter, 1990 for acoustical details) four times a day on the first and second days following hatching and again at 8 A . M . on the day of testing. In other words, chicks received a total of 405 min of auditory stimulation over the course of the first 3 days following hatching. The contentment call recording was obtained from observations of socially reared bobwhite hatchlings in a previous study (see McBride & Lickliter, 1993). The prepared tape loop was played on a Marantz model PMD 221 portable cassette recorder and was presented at auniform peak intensity of 65 db, as measured by a Bruel and Kjear Model 2232 sound level meter.

Twenty-one chicks were individually tested in a simultaneous choice test between a bobwhite maternal call and a chicken maternal call at 72 hr following hatching (auditory group). Twenty-five subjects were individually tested in a simultaneous choice test between a bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen (visual group). As in the previous experiment, because both the bobwhite hen and the scaled hen were emitting the same auditory cue (i.e., the bobwhite maternal call), subjects in this group were required to base their preferential responding on the available visual cues provided by the hens. Choice, latency, and duration were scored as described in the General Methods section.

Results and Discussion The results of testing are shown in Tables 1 and 2. Chicks that were tested in the

auditory test between the bobwhite maternal call and the chicken maternal call did not show a high degree of responsiveness for the bobwhite maternal call (Table I ) . Only 8


of 25 birds tested (32%) responded during the trial. Of the 8 chicks that responded during testing, 7 preferred the bobwhite maternal call, paralleling the results obtained from control chicks in Experiment 1 .

Chicks that were tested in the visual test between the bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen showed a significant preference for the bobwhite maternal call paired with the stuffed model of the bobwhite hen at 72 hr following hatching, p < .05, Table 2. Correspondingly, there were significantly shorter latencies, p < .001, and longer duration scores, p < .01, in the subjects’ responses to the bobwhite maternal call paired with the model of the bobwhite hen.

These results show that postnatal exposure to augmented amounts of bobwhite hatchling contentment calls does not serve to alter bobwhite chicks’ species-typical responsiveness to maternal auditory or visual cues. It may be that the type of auditory experience to which chicks are exposed is more important in affecting chicks’ postnatal responsiveness than the amount of auditory stimulation. To assess the possibility that the type of stimulation is more important than amount of stimulation in affecting chicks’ perceptual responsiveness, chicks in the next experiment were exposed to augmented amounts of a different type of auditory stimulation. Specifically, chicks were exposed to recordings of bobwhite hatchling distress calls during the first 3 days following hatching. Unlike bobwhite contentment calls, this type of vocalization is not typically present in socially reared bobwhite chicks’ posthatch environment (McBride & Lickliter, 1993).

Experiment 3: Auditory and Visual Responsiveness of Chicks Exposed to Bobwhite Distress Calls

Method Forty-six bobwhite quail chicks, drawn from three separate hatches, served as

subjects. Following hatching, all chicks were placed in social groups containing 12-18 same-aged chicks and were exposed to 45 min of recorded bobwhite hatchling distress vocalizations (characterized by long note durations and high pitch, see Stoumbos & Lickliter, 1990 for acoustical details) four times a day (beginning at 8 A . M . , 12 noon, 4 P . M . , and 8 P .M. ) on the first and second days following hatching and again at 8 A . M .

on the day of testing. In other words, subjects received a total of 405 min of distress- call stimulation over the course of the first 3 days following hatching. The recordings of bobwhite chick distress calls were obtained during the course of observations of isolate-reared bobwhite hatchlings in a previous study (McBride & Lickliter, 1993).

Twenty-one chicks were individually tested in a simultaneous choice test between the bobwhite maternal call and a chicken maternal call at 72 hr following hatching (auditory group). Twenty-five subjects were individually tested in a simultaneous choice test between a bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen as in Experiments 1 and 2 (visual group). Choice, latency, and duration were scored as described in the General Methods section.

Results and Discussion The results of this experiment are shown in Tables 1 and 2. Chicks that were tested

in a simultaneous choice test between the bobwhite maternal call and the chicken maternal call did not show a reliable pattern of responsiveness to the bobwhite maternal

AUDITORY STIMULATION AND VlSUAL RESPONSIVENESS 177

call (Table 1). Only 10 of 25 chicks tested (40%) responded during testing. Of the 9 that did respond, 8 chicks preferred the bobwhite maternal call over the chicken maternal call, paralleling the results obtained from control chicks in Experiments 1 and 2 (Table 1).

Chicks that were tested in the simultaneous choice test between the bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen did not show a preference for either the bobwhite hen model paired with the bobwhite maternal call or the scaled quail hen model paired with the bobwhite maternal call (Table 2 ) . Correspondingly, there were no significant differences in latency scores or duration scores for either stimulus array.

These results indicate that exposure to bobwhite hatchling distress vocalizations during the first 72 hr following hatching does not alter chicks’ typical patterns of auditory responsiveness to maternal cues, but does interfere with chicks’ species-typical responsiveness to maternal visual cues. When compared to the results of Experiment 2 , the findings of this experiment demonstrate differential effects of bobwhite distress call exposure versus bobwhite contentment call exposure and suggest that the type of postnatal auditory stimulation provided is a critical factor in influencing chicks’ subsequent perceptual functioning. A similar conclusion was reached in a study of the effects of prenatal auditory stimulation (Lickliter & Stoumbos, 1991). In that study, only specific types of prenatal auditory stimulation were found to alter chicks’ subsequent postnatal visual responsiveness.

To further test the notion that only specific types of postnatal auditory stimulation interfere with perceptual functioning, the next experiment exposed bobwhite chicks to domestic chicken (Gallus domesticus) hatchling distress calls. Unlike the auditory stimulation presented in Experiments 2 and 3, this stimulation regime consisted of exposure to species-atypical (nonconspecific) auditory experience.

Experiment 4: Auditory and Visual Responsiveness of Chicks Exposed to Chicken Hatchling Distress Calls

Method Forty-three bobwhite quail chicks, drawn from three separate hatches, served as

subjects. Following hatching, all chicks were placed in social groups containing 12-18 same-aged chicks and were exposed to 45 min of recorded domestic chicken hatchling distress calls four times a day on the first and second days following hatching and again at 8 A . M . on the day of testing. As in Experiments 2 and 3, chicks received a total of 405 min of auditory stimulation over the course of the first 3 days following hatching. The chicken distress call recording was obtained from an isolated 8-day-old chicken hatchling.

Eighteen bobwhite chicks were individually tested in a simultaneous choice test between the bobwhite maternal call and a chicken maternal call at 72 hr following hatching (auditory group). Twenty-five subjects were individually tested in a simultaneous choice test between a bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen (visual group). Choice, latency, and duration were scored as described in the General Methods section.

Results and Discussion The results of testing are shown in Tables 1 and 2 , Chicks that were tested in the

auditory test between the bobwhite maternal call and the chicken maternal call did not show a consistent pattern of responsiveness for the bobwhite maternal call (Table 1).


Only 7 of 18 birds tested (39%) responded during the trial. Of the 7 chicks that responded during testing, all preferred the bobwhite maternal call, paralleling the results of Experi- ments I , 2, and 3.

Chicks that were tested in the visual test between a bobwhite maternal call paired with a stuffed bobwhite hen and the same bobwhite maternal call paired with a stuffed scaled quail hen showed a significant preference for the bobwhite maternal call paired with the stuffed model of the bobwhite hen at 72 hr following hatching, p < .OS, Table 2. Correspondingly, there were significantly shorter latencies, p < .001, and longer duration scores, p < .01, in the subjects’ responses to the bobwhite maternal call paired with the model of the bobwhite hen, paralleling the results of Experiments 1 and 2 .

These results show that postnatal exposure to chicken hatchling distress vocalizations does not serve to alter bobwhite chicks’ species-typical responsiveness to maternal auditory or visual cues. These findings further support the notion that augmented postnatal auditory stimulation, in and of itself, is not sufficient to interfere with subjects’ perceptual responsiveness. Rather, exposure to a specific type of auditory stimulation, the bobwhite distress call, is apparently necessary to interfere with the development of species-typical visual responsiveness (Experiment 3).

In this light, it is interesting to note that several recent studies utilizing bobwhite quail chicks (McBride & Lickliter, 1993), ducklings (Gottlieb, 1991, 1993), and domestic chicks (Gray, 1990) have indicated that excessive arousal of precocial avian hatchlings can interfere with species-typical perceptual responsiveness. Given that chicks exposed to distress calls in Experiment 3 did not respond to species-specific visual cues and chicks in this experiment and Experiments 1 and 2 did respond in a species-typical fashion, it seems possible that exposing chicks to distress calls over the course of the first 3 days following hatching resulted in increased levels of arousal, which may have interfered with the birds’ developing visual abilities. To further examine this possibility, the next experiment compared the behavior of chicks during exposure to distress calls with that of chicks exposed to contentment calls during the days following hatching in an attempt to assess behavioral arousal levels across exposure conditions.

Experiment 5: Observations of Chicks Exposed to Distress Calls, Contentment Calls, and Chicken Calls Few studies on the effects of sensory or social experience in young animals have

provided details of how the infants actually behave when in the presence of increased (or decreased) levels of experiential stimulation. Rather, most studies of early experience have focused exclusively on what happens later at a single point in time (King & West, 1987). In the present experiment, chicks in each stimulation condition were observed during baseline periods and during exposure to auditory stimulation prior to testing in an attempt to assess the behaviors and arousal levels associated with each auditory exposure condition that may have contributed to the subjects’ behavior during the testing trials.

Method We observed 12 chicks from each auditory stimulation group (bobwhite contentment

call, bobwhite distress call, and chicken distress call) for 20 min twice each day during the first and second days following hatching. Each observation period consisted of a 5-min baseline, 5 rnin of auditory stimulation (recordings of either bobwhite distress


Table 3 Percentage of Time Spent in Each Activity During Behavioral Observations

~

Auditory Stim Eyes Open Proximity Contact Movement ~

Control Group 100 .98 .88 .37 Bobwhite Contentment I00 .97 .86 .44 Call Group Bobwhite Distress Call 100 .98 .86 .41 Group Chicken Distress Call .99 .99 .85 .47 Group

calls, bobwhite contentment calls, or chicken hatchling distress calls), 5 min poststimula- tion, and a second 5-min auditory stimulation period. Data were recorded on checksheets which included (a) whether the subject’s eyes were open or closed, (b) whether the subject was alone or in physical proximity (within one body length) of 2 or more hatchlings, (c) whether the subject was in direct physical contact with at least 1 other hatchling, and (d) whether the subject was engaged in locomotor activity.

In addition, the number of distress vocalizations emitted was recorded for each group. This was accomplished by placing a Marantz (model #PMD221) cassette tape recorder next to the rearing tub and recording the number of distress vocalizations emitted from the three stimulation groups during the baseline and stimulation periods.

Finally, the auditory stimuli (bobwhite distress calls, bobwhite contentment calls, and chicken hatchling distress calls) were acoustically analyzed with a bioacoustic software program (SIGNAL) in order to obtain time signals and spectrograms of the three calls. Previous work has shown that precocial avian embryos and hatchlings are particularly sensitive to the repetition of rate of species-specific vocalizations (Gottlieb, 1981). For example, Miller (1983) examined repetition rates of mallard duck calls and found that slow repetition rates promoted behavioral inhibition in ducklings and faster repetition rates promoted behavioral excitation in mallard ducklings. Higher repetition rates may be more arousing to chicks and thus may be an important feature of the distress vocalizations which interfere with chicks’ development of species-typical visually guided responsiveness. To examine this possibility, the repetition rate for each of the three calls used in this study was examined by calculating the number of notes emitted per second within a single burst by the formula recommended by Scoville and Gottlieb (1978). This formula is R = n - 1/L, where N is the number of notes in the call, and L is the duration of the call in seconds measured from the beginning of the first note to the beginning of the last note.

Results and Discussion Table 3 shows the percentage of time that subjects in each stimulation condition

spent engaged in each of the recorded behaviors. Multiple comparisons revealed no significant differences between groups for the amount of time spent with eyes open, time spent moving, or time in proximity or in contact with others. All of the subjects in each group spent the majority of the 20-min observation period with their eyes open


Table 4 Distress Vocalizations Emitted by Subjects at 24 and 48 hr Following Hat c hing Auditory Stimulation Age (hr) Baseline Stim Poststim Stim

Bobwhite Contentment 24 0 0 0 0 Call 48 0 0 0 0 Bobwhite Distress 24 0 51 4 13 Call 48 0 0 0 0 Chicken Distress 24 0 0 0 0 Call 48 0 0 0 0

(suggesting that they were awake during the observation period). Subjects in each condition spent the majority of observation time in physical proximity to 2 or more other hatchlings. In addition, subjects were in direct physical contact with at least 1 other hatchling for the majority of observation time (Table 3). In sum, subjects in each condition spent the majority of the 20-min observation period huddled together in a group of broodmates.

Table 4 shows the number of distress vocalizations emitted by each group during the baseline and stimulation periods at 24 and 48 hr. Results showed that subjects in the control group, bobwhite contentment call group, and chicken distress call group did not emit distress vocalizations during the observation periods. Only chicks exposed to bobwhite distress calls were observed to emit distress calls. These distress vocalizations occurred primarily during the auditory stimulation period, and were only observed at 24 hr following hatching (Table 4).

These findings are consistent with previous observations which revealed that un- stimulated, group-reared bobwhite quail chicks do not typically emit distress vocalizations (McBride & Lickliter, 1993). These findings are also consistent with previous findings obtained from ducklings (Gaioni & Platte, 1982), in which ducklings were found to attend to other ducklings’ distress vocalizations and alternately respond with their own distress calls. Gaioni (1982) also found that this alternation of distress calls was elicited by the presentation of either live or recorded distress calls and was facilitated by visual contact with a conspecific.

In a similar vein, McBride and Lickliter (1993) found that partially isolated bobwhite chicks (i.e., chicks had the opportunity to see one sibling through a glass divider) frequently emit distress calls during the first 72 hr following hatching. Furthermore, partially isolated chicks do not exhibit species-typical visual responsiveness for the bobwhite hen at 72 hr of age, paralleling the results of Experiment 3 . One explanation for this finding may be that the potentially distracting stimulation from the subjects’ own distress calling interfered with the chicks’ attentiveness to visual experience with conspecifics, which has been found to be necessary for the development of visually based maternal recognition (McBride & Lickliter, 1993). In particular, distress calling may be indicative of the subjects’ high state of arousal (Gray, 1990), which may serve to interfere with the chicks’ attentiveness to visual experience with conspecifics (see Gottlieb, 1993 for a similar auditory example with ducklings).


Acoustic analysis of the three stimulation calls revealed that the bobwhite distress call had a higher repetition rate, R = 3.9 notes per second, than either the bobwhite contentment call, R = 2.4 notes per second, or the chicken distress call, R = 2.3 notes per second. This difference suggests that repetition rate may be the critical acoustical variable in affecting chicks’ development of species-typical visual responsiveness seen in Experiment 3 . On the other hand, acoustic features such as bandwidth or frequency modulation may also prove to be important factors in affecting chicks’ perceptual responsiveness. Future research and acoustic analyses are required to assess these possibilities.

General Discussion The results of this study demonstrate that augmentation of auditory experience can

result in deficits or abnormalities in typical patterns of early perceptual development. In particular, the results indicate that postnatal exposure to bobwhite chick distress calls interferes with bobwhite chicks’ subsequent species-typical responsiveness to maternal visual cues (Experiment 3). In contrast, postnatal exposure to augmented amounts of bobwhite hatchling contentment vocalizations or chicken hatchling distress vocalizations did not interfere with chicks’ auditory or visual responsiveness (Experi- ments 2 & 4). These findings indicate that exposure to increased amounts of auditory stimulation during the early postnatal period is not sufficient, in and of itself, to interfere with subsequent perceptual functioning. Rather, the type of auditory stimulation presented appears to be the more important factor in affecting early perceptual preferences.

Results from previous studies of bobwhite chicks also support this view. For example, Lickliter and Stoumbos (1991) found that prenatal exposure to augmented auditory stimulation altered bobwhite chicks’ postnatal visual responsiveness to maternal cues, but only when prenatal auditory stimulation was comprised of specific repetition rates. In other words, not all forms of prenatal auditory experience were effective in altering subsequent perceptual development. Similarly, Lickliter and Stoumbos (1992) showed that only certain types of prenatal auditory experience were sufficient to alter bobwhite chicks’ postnatal auditory responsiveness to maternal cues. Chicks that received increased amounts of exposure to unaltered repetition rates of bobwhite embryonic vocalizations prenatally showed species-typical patterns of auditory responsiveness to maternal cues, whereas chicks exposed to altered repetition rates showed atypical patterns of auditory responsiveness. Interestingly, repetition rate has emerged as an important acoustic variable for precocial avian hatchlings across both prenatal and postnatal studies (Gottlieb, 1981; Miller, 1983).

Taken together, the results of these studies and the present study suggest that type of sensory stimulation, rather than simply amount of stimulation, is the more important factor in determining effects on perinatal perceptual development. Of course, this is not to say the amount of sensory stimulation is not a factor in affecting early perceptual organization. Amount and type of stimulation may have a quantitatively modifying effect on early perceptual development, and the nature of such modification is likely to be limited or constrained by system-specific thresholds (Radell & Gottlieb, 1992). Modifications in sensory experience that go beyond such thresholds could serve to interfere with both intra- and intersensory functioning. In this light, Radell and Gottlieb (1992) have recently argued that experimental manipulations that expose subjects to species-typical or mildly enhanced levels of sensory experience should result in typical or even facilitated intersensory development, whereas greatly augmented or deprived


sensory stimulation should result in deficits in intersensory development. The results of the present study imply that the type of sensory stimulation provided should also be incorporated into this threshold scenario.

Behavioral observations and acoustic analysis (Experiment 5 ) yielded results that may account for the differential effects of the various hatchling calls on perceptual functioning. Specifically, only hatchlings exposed to bobwhite distress calls emitted their own distress calls during exposure. Therefore, bobwhite hatchlings that are exposed to bobwhite distress calls experienced not only the additional experimental auditory stimulation, but also their own vocalizations and the vocalizations of other hatchlings in the brood during the exposure period. This additional auditory experience and/or the experience of vocalizing may account, at least in part, for the visual lack of typical responsiveness seen in Experiment 3. As stated previously, prior research with precocial avian hatchlings has suggested that distress vocalizations may be indicative of higher behavioral arousal (Gottlieb, 1993; Gray, 1990). In the present study, behavioral arousal may have been induced by the high repetition rate of the bobwhite distress calls, and this increased arousal may have somehow interfered with the young chicks’ intersensory functioning. These, of course, remain speculations at present and point to the need for future research in which the role of arousal levels in early perceptual development is examined more fully. In addition, future studies should involve the manipulation of repetition rates of hatchlings’ calls in order to further investigate the specific roles of type and amount of auditory stimulation in perinatal perceptual development and organization.

Notes This research was supported by NIMH Grant MH48949 awarded to Robert Lickliter. We followed both

national and institutional guidelines for the care and use of animal subjects. We thank Robyn Krutchkoff, Leslie Lipscomb, Dan MacKay, Ed Laurent, and Alice Nair for assistance with data collection and acoustical analyses.

References

Banker, H . , & Lickliter. R. (1993). Effects of early and delayed visual experience on perceptual development

Gaioni, S . J . (1982). Distress call alternation in Peking ducklings (Anas platyrhynchos). Animal Behuuiour,

Gaioni, S . J . , & Platte, P. L. (1982). Sibling interactions in mallard ducklings (Anas platyrhynchos). Animul

Gottlieb, G . (197 I ) . Development of species identification in birds. Chicago: University of Chicago Press. Gottlieb, G. (1981). Roles of early experience in species-specific perceptual development. In R. N. A s h ,

J. R . Alberts, & M. R . Peterson (Eds.), Developnieiit of perception, (Vol. I , pp. 5-44). New York: Academic Press.

in bobwhite quail chicks. Developmental Psychobiology, 26, 155-170.

30, 774-789.

Behauiour Letters, 2, 189-196.

Gottlieb, G. (1991). Social induction of malleability in ducklings. Animal Behauiour, 41, 953-962. Gottlieb, G . (1993). Social induction of malleability in ducklings: Sensory basis and psychological mechanism.

Gray, L. (1990). Activity level and auditory responsiveness in neonatal chickens. Developmental Psychobiol-

Heaton, M. B., Miller, D. B., & Goodwin, D. G. (1978). Species-specific auditory discrimination in bobwhite

Johnsgrad, P. A. (1973). Grouse and quails of Norrh America. Lincoln, NE: University of Nebraska Press. King, A. P., & West, M. J. (1987). The experience of experience: An exogenetic program for social compe-

tence. In P. P. G. Bateson & P. H. Klopfer (Eds.), Perspectives in ethology (pp. 153-182). New York: Plenum Press.

Animul Behaviour, 43, 707-719.

ogy, 23, 297-308.

quail neonates. Developmental Psychobiology, 11, 13-21.


Lickliter, R. (1990a). Premature visual stimulation accelerates intersensory functioning in bobwhite quail neonates. Developmental Psychobiology, 23, 15-27.

Lickliter, R. (1990b). Premature visual experience facilitates visual responsiveness in bobwhite quail neonates. Infant Behavior and Development, 13, 487-496.

Lickliter, R. (1993). Timing and the development of perinatal perceptual organization. In G . Turkewitz & D. A. Devenny (Eds.), Developmental time and riming (pp. 105-123). Hillsdale, NJ: Erlbaum.

Lickliter, R. (in press). Prenatal visual experience alters postnatal sensory dominance hierarchy in bobwhite quail chicks. Znfunt Behavior and Development.

Lickliter, R., & Stoumbos, J . (1991). Enhanced prenatal auditory experience facilitates postnatzal visual responsiveness in bobwhite quail chicks. Journal of Comparative Psychology, 105, 89-94.

Lickliter, R., & Stoumbos, J . (1992). Modification of prenatal auditory experience alters postnatal auditory preferences of bobwhite quail chicks. Quarterly Journal of Experimentul Psychology. 44B, 199-214.

Lickliter, R., & Virkar, P. (1989). Intersensory functioningin bobwhite quail chicks: Early sensory dominance. Developmental Psychobiology, 22, 65 1-667.

McBride, T. C., & Lickliter, R. (1993). ViSudl experience with siblings fosters species-specific responsiveness to maternal visual cues in bobwhite quail chicks (Colinus virginianus). Journal of Comparative Psycho/-

Miller, D. (1983). Alarm call responsivity of mallard ducklings: 11. Perceptual specificity along an acoustical dimension affecting behavioral inhibition. Developmental Psychobiology, 16, 195-205.

Radell, P. L., & Gottlieb, G . (1992). Developmental intersensory interference: Augmented prenatal sensory experience interferes with auditory learning in duck embryos. Developmental Psychology, 28, 795-803.

Scoville, R., & Gottlieb, G. (1978). The calculation of repetition rate in avian vocalizations. Animal Behauiour,

Stokes, A. W. (1967). Behavior of the bobwhite (Colinus virginianus). Auk, 84, 1-33. Stoumbos, J . , & Lickliter, R. (1990). Acoustic features of the embryonic vocalizations of bobwhite qunil.

o g y , 107, 320-327.

26, 962-963.

Unpublished manuscript, Virginia Polytechnic Institute and State University, Blacksburg.

Specific postnatal auditory stimulation interferes with species-typical visual responsiveness in...

Documents

Transcript of Specific postnatal auditory stimulation interferes with species-typical visual responsiveness in...