type and amount of prenatal stimulation alters perceptual responsiveness in bobwhite quail chicks

INFANT BEHAVIOR AND DEVELOPMENT 19,325-338 (1996)

Type and Amount of Prenatal Stimulation Alters Perceptual Responsiveness in Bobwhite Quail Chicks

MERRY J. SLEIGH AND ROBERT LICKLITER Virginia Polytechnic Institute and State University

To explore the relationship between the type and amount of sensory stimulation provided prenatally and its impact on postnatal responsiveness to maternal cues, bobwhite quail embryos were exposed to 5 or 10 min/hour of either bobwhite chick contentment calls or bobwhite chick distress calls. Results revealed that embryos exposed to 5 or 10 min/hour of distress calls continued to respond to maternal auditory cues into later stages of postnatal development in comparison to controls and failed to demonstrate species-typical responsiveness to maternal visual cues. In contrast, embryos exposed to 5 min/hour of contentment calls continued to respond to maternal auditory cues into later stages of development and exhibited species-typical patterns of visual responsiveness (72 hour of age). Embryos exposed to 10 min/hour of contentment calls responded to maternal auditory cues into later stages of postnatal development but showed an accelerated responsiveness to maternal visual cues (48 hours of age). Taken together, these results suggest that the type and amount of sensory stimulation interact during the prenatal period to influence the course of perceptual development.

prenatal experience intersensory perception early perceptual organization intermodal interference and facilitation

Departures from normal or usual sensory experience during the prenatal period can exert important influences on subsequent perceptual organization (Banker & Lickliter, 1993; Gottlieb, Tomlinson, & Radell, 1989; Lickliter, 1994; Radell & Gottlieb, 1992). For example, Lickliter (1990a, 1990b) has shown that unusu- ally early (prenatal) visual stimulation can accelerate the emergence of intersensory responsiveness in bobwhite quail chicks. Likewise, Lickliter and Stoumbos (1991) have shown that augmented prenatal auditory stimulation can also result in accelerated intersensory functioning in bobwhite chicks in the days following hatching. These demonstrations of the effects of alterations in prenatal sensory experience on subsequent perceptual organization illustrate that normal or usual postnatal perceptual development is a consequence of normal

This research was supported in part by NIMH Grant MH48949, awarded to R.L. We thank Michael Casey, Rebecca Columbus, Brad Hughston, Leslie Lipscomb, Deanna McCullers, and Kathleen Savage for their assistance with data collection and Darren Ritzer for his statisti- cal assistance. We followed both national and institutional guidelines for the care and use of animal subjects.

Correspondence and requests for reprints should be sent to Robert Lickliter, Department of Psychology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061436.

prenatal experience and raise questions about the critical aspects of the stimulation that mediate shifts in early intersensory relationships.

In this light, results from a number of studies with precocial birds suggest that the effect(s) that manipulations of perinatal sensory stimulation might have on early perceptual development is likely to depend on a number of nested factors, including the timing of the stimulation relative to the stage of the organism, the amount of stimulation provided or denied, and the type of sensory stimulation presented to the young organism (Gottlieb, 1971, 1993; Lickliter & Lewkowicz, 1995; McBride & Lickliter, 1993, 1994; Radell & Gottlieb, 1992). These factors and their influence are likely to interact in mul- tiplicative ways and to change with the organism’s context, the organism’s state, and the organism’s developmental history (Gardner, Lewkowicz, Rose, & Karmel, 1986; Lewkowicz & Turkewitz, 1980, 1981).

A key factor likely associated with the influence of sensory experience on early perceptual development is the amount of stimulation that the developing organism encounters. Based on their findings from enhanced vestibular stimulation in duck embryos, Radell and Gottlieb (1992) recently argued that the amount of stimulation an organism encounters in its typical developmental context may be optimal for its species-specific

325

326 Sleigh and Lickliter

perceptual development. In other words, sensory experience that falls within a range of stimulation typical for that species should not interfere with intersensory development, and mildly enhanced levels of stimulation may maintain or even facilitate typical perceptual development. This hypoth- esis would potentially explain the findings of Lickliter (1990a), in which enhanced prenatal visual stimulation led to accelerated intersensory functioning. However, if some optimal range of stimulation exists, then stimulation that exceeds that optimal range should potentially cause functional deficits in normal patterns of intersensory functioning.

Recent work with precocial birds lends support to the existence of some optimal range of perinatal stimulation necessary for species- typical perceptual development (Gottlieb et al., 1989; Lickliter & Lewkowicz, 1995; Sleigh & Lickliter, 1995). For example, Lickliter and Hellewell (1992) have shown that bobwhite embryos exposed to a particular variant of a bobwhite maternal call demonstrate the ability to learn the call when the call is presented nonconcurrently with 10 min/hour of patterned light. In contrast, embryos do not exhibit this auditory learning ability when the maternal call is presented concurrently with the light. In a similar vein, Radell and Gottlieb (1992) demonstrated that mallard duckling embryos failed to learn an individual mallard maternal call when exposed concurrently to waterbed stimulation, but did demonstrate auditory learning ability when the amount of waterbed stimulation was reduced to more closely approximate their normal range of prenatal vestibular stimulation. Taken together, these findings suggest that when overall amounts of stimulation exceed a certain level, early auditory learning can be compromised.

In addition to amount of stimulation, the effects of sensory stimulation may be simulta- neously influenced by the specific type of stimulation to which the developing organism is exposed. For example, Lickliter and Stoumbos ( 1991) found that only certain types of enhanced prenatal auditory stimulation serve to facilitate chicks’ species-specific visual responsiveness. Specifically, when bobwhite quail embryos were exposed to increased amounts of vocalizations that typically occur in the late prenatal environment (bobwhite chick contentment calls), postnatal visual functioning was

accelerated. In contrast, bobwhite quail embryos exposed to bobwhite embryonic vocalizations with a faster repetition rate than normal did not show this accelerated pattern of postnatal visual responsiveness (Lickliter & Stoumbos, 1991), indicating that type of stimulation can be an important variable in under- standing how sensory experience mediates subsequent perceptual functioning. In addition, this finding raises the possibility that type may serve a mediating role in determining what con- stitutes an optimal amount of stimulation. In other words, the level of stimulation needed to maintain or facilitate species-typical development may depend, at least to some extent, on the type of sensory stimulation the embryo encounters during the prenatal period.

This possibility of differential effects dependent on type of stimulation appears to be the case in the early postnatal environment. For example, McBride and Lickliter (1994) exposed bobwhite quail hatchlings to augmented amounts of bobwhite chick distress calls, bobwhite chick contentment calls, or domestic chicken distress calls during the first 72 hours following hatching. Bobwhite hatchlings exposed to either bobwhite chick contentment calls or domestic chicken distress calls demonstrated species-typical auditory and visual responsiveness to maternal cues at 72 hours following hatching. In contrast, bobwhite hatchlings exposed to bobwhite chick distress calls did not exhibit species-typical visual responsiveness to maternal cues, suggesting that specific types of auditory stimulation differentially impact early postnatal perceptual functioning.

In sum, the effect that a manipulation of sensory experience may have on perinatal 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 stimulation provided. As a first step in examining the interactions between these factors during the prenatal period, this study assessed the effects of different amounts of two types of species-typical prenatal auditory stimulation on the development of species- specific perceptual responsiveness in bobwhite quail chicks. In particular, this study was designed to explore whether the range of stimulation that results in normal perceptual organization shifts as a consequence of the type of stimulation presented.

Effects of Prenatal Auditory Stimulation 327

GENERAL METHODS

Certain features of the experimental design were common to all experiments, so these features are described first before presenting the particular details of each experiment.

Subjects

Subjects were 480 maternally naive, incubator-reared bobwhite quail embryos (Colinius ~ir&ianus), 120 of which participated in each of four experiments. Fertile, unincubat- ed eggs were received weekly from a commercial supplier and were set in a Petersime Model I incubator, maintained at 37.YC and 85% humidity. After 20 days of incubation, the eggs were transferred to a hatching tray located in the bottom of the incubator (bobwhite quail typically hatch between Day 22 and Day 23). Only those birds that hatched during Day 23 were used as subjects to control for possible effects of variations in developmental age. The embryo’s age is calculated on the basis of the first day of incubation being Day 0, the second 24 hours of incubation being Day I, and so on. The possible influence of between-batch vari- ation in behavior was controlled by drawing subjects for each experimental group from three or more different batches (i.e., weeks) of eggs. After hatching, subjects were reared in groups of 10 to 12 same-age chicks to mimic naturally occurring brood conditions. As a result of their incubation rearing, the only sounds to which chick embryos and hatchlings were exposed until the time of experimental manipulation or testing were their own embryonic and postnatal vocalizations (and those of their broodmates) and the low-frequency background noises emanating from the incubator fan and motor. The sound-attenuated room in which the hatchlings were reared was illuminated by a 100-W brooder lamp suspended above each plastic rearing tub, which maintained an ambient air temperature of approximately 3O’C.

Procedure

To ensure that the embryos could hear the enhanced auditory stimulation, during the second half of the 21st day of incubation, a portion of the shell and the inner shell membrane over the air space of the egg of each subject was removed. The embryo’s bill usually penetrates the air space of the large end of the egg early on Day 2 1, and at this time the embryo begins to respire and vocalize (Freeman & Vince, 1974). As a result, removing a small portion of the shell does not affect postural orientation, incubation. sur- vivability, or species-typical perceptual behavior (Banker & Lickliter, 1993; Lickliter, 1990a). Following the egg- opening procedure, opened eggs were placed in a portable, Hovi-bator incubator. Temperature and humidity were maintained as before.

Embryos were stimulated with either bobwhite distress vocalizations or bobwhite contentment vocalizations for either IO min each hour during the last 24 hours prior to hatching (total exposure time = approximately 240 min) or for 5 min each hour during the last 24 hours prior to hatching (total exposure time = 120 min). The recording of bobwhite chick distress calls was obtained during the course of observations of isolate-reared bobwhite hatchlings in a previous study (McBride & Lickliter, 1993; see Stoumbos & Lickliter. 1990, for acoustical details). The recording of the bobwhite chick contentment calls was obtained during the

course of observations of normally reared bobwhite hatchlings (see Stoumbos & Lickliter, 1990, for acoustical details). The bobwhite chick calls were broadcast via a Maranta PMD 221 cassette tape recorder at a uniform peak intensity (65 dB), measured by a Bruel and Kjaer Model 2232 (B-weighted scale, fast-response) sound-level meter.

Testing

Testing occurred at 24,48,72, or 96 hours (? 3 hours) after hatching. Testing occurred in a circular arena, 160 cm in diameter, surrounded by a wall 24 cm in height and draped by an opaque black curtain to shield the observer from the subject’s view. The walls of the apparatus were lined with foam to attenuate echoes, and the floor was painted tlat black. Two rectangular approach areas (32 cm x 15 cm) were demarcated on opposite sides of the arena by green stripes painted on the floor. These approach areas made up less than 5% of the total area of the arena. A midrange dome-radiator speaker was positioned behind the curtain in each of the approach areas, equidistant from the point at which each subject was placed in the apparatus. Each speaker was connected to a Tascam model 122-B cassette tape recorder located on a control table. The observer, drawn from trained undergraduates blind to the experimental design, sat at this table and observed each subject’s activities through a large mirror positioned above the arena. A system of stop watches was used to score latency and duration of response.

During testing, each quail chick was placed singly in the test apparatus equidistant from the two approach areas. During the 5-min test, subjects were scored on both latency of approach and duration of time spent in each of the two approach areas. In the simultaneous-choice test, the loca- tions of the stimuli presented were alternated between subjects to prevent any possible side bias from intluencing results. Each subject was tested only once, and latency was scored as the amount of time (in seconds) that elapsed from the onset of the trial until the bird entered an approach area. Duration was scored as the cumulative amount of time (in seconds) the subject remained in an approach area during the 5-min test. A chick that did not enter an approach area received a score of 300 s latency (the length of the trial) and 0 s for duration for that stimulus and was considered a “nonresponder.” A chick that stayed in one approach area for more than twice the time it spent in the opposing approach area over the course of the 5-min trial was scored with a preference for that stimulus. A chick that approached both approach areas during a test without showing a preference for either one wan scored as “no preference.” This measure of preference yielded a convenient summary of the behavior of each bird in the various experimental groups.

Data Analysis

The primary data of interest were measures of preference for the auditory and visual stimuli presented during the tri- als. Three such measures of preference were analyzed: (a) Differences in the latency of approach to each stimulus by a subject in a group were evaluated by the Wilcoxon matched-pairs signed-ranks test: (b) differences in the duration of time spent in each approach area by a subject in a group were evaluated by the Wilcoxon matched-pairs signed-ranks test; and (c) an individual preference. derived from duration of response and assigned to any subject that


stayed in one area for more than twice as long as the other approach area, was evaluated by a chi-square test. Significance levels of p < .05 were used to evaluate results.

EXPERIMENT 1

Effects of 10 Min/Hour of Prenatal Exposure to Bobwhite Contentment Calls or Bobwhite Distress Calls on Postnatal

Auditory Responsiveness

As previously discussed, McBride and Lickliter ( 1994) demonstrated that bobwhite chicks respond differently to hatchling contentment calls versus hatchling distress calls when the calls are presented in the days immediately following hatching. Specifically, augmented postnatal exposure to the distress call led to deficits in chicks’ normal patterns of perceptual functioning, whereas augmented postnatal exposure to the contentment call did not. The influence of type of stimulation may be even more powerful during the prenatal period, when the emerging sensory systems are becoming functional.

During the late stages of the prenatal period, quail embryos’ vocalizations typically consist of infrequent contentment vocalizations (Sleigh, 1994). In contrast, embryos do not typically emit or experience bobwhite hatchling distress calls during this time. Thus, one type of auditory stimulation employed in this study is typically present in the embryos’ prenatal environment (contentment vocalizations), whereas the other type of auditory stimulation employed distress vocalizations is typically rare or absent in the embryos’ prenatal environment. Recall that Lickliter and Stoumbos (1991) were able to accelerate species-typical perceptual development by providing embryos’ with augmented amounts of naturally occurring bobwhite chick contentment calls in the days prior to hatching.

If the amount of stimulation overrides the type of stimulation provided, then bobwhite quail embryos exposed to 10 min/hour of bobwhite chick distress calls during the final 24 hours prior to hatching should appear similar to embryos exposed to 10 min/hour of bobwhite chick contentment vocalizations; specifically, these subjects should demonstrate accelerated visual responsiveness to maternal cues. If the amount of stimulation which falls within some optimal range is mediated by the type of stimulation, then bobwhite quail embryos exposed to

10 min/hour of bobwhite distress calls during the period prior to hatching should demonstrate altered patterns of perceptual development, as compared to embryos exposed to 10 mitt/hour of bobwhite contentment calls.

Method

Subjects were 120 bobwhite quail embryos, drawn from 18 separate hatches. The shell and membrane over the air space of the egg of each subject were removed as described in the GENERAL METHODS section. After this procedure, subjects were incubated in groups of 10 to 12 same-aged embryos. Subjects were stimulated for 10 min/hour for a minimum of 24 hours from the second half of Day 21 to the second half of Day 22 of incubation. Sixty embryos were exposed to recorded bobwhite hatchling contentment vocalizations (see Stoumbos & Lickliter, 1990, for acoustical details). A second group of 60 embryos was exposed to bobwhite hatchling distress vocalizations (characterized by long note duration and high pitch; see Stoumbos & Lickliter, 1990, for acoustical details). To determine if either of these prenatal manipulations affected hatchlings’ species-typical auditory preference for the maternal call, subjects in each condition were given a simultaneous-choice test between a bobwhite maternal call and a chicken maternal call (see GENERAL METHODS) at either 24 hours (n = 20 from contentment call group, and n = 20 from distress call group), 72 hours (n = 20 from contentment call group, and n = 20 from distress call group) or 96 hours (n = 20 from contentment call group, and n = 20 from distress call group) following hatching. Previous studies have revealed that unmanipulated chicks show a naive auditory preference for the bobwhite maternal call over species-atypical maternal calls at both 24 and 48 hours following hatching, but require combined maternal auditory and maternal visual cues to direct social preferences by 72 hours following hatching. During testing, the calls were broadcast at a uniform peak intensity (65 dB, B-weighted scale, fast response), measured by a sound-level meter at the point where the chick was intro- duced into the arena. Acoustical details of the calls are provided by Heaton, Miller, and Goodwin (1978) and Gootlieb (1971).

Results and Discussion

Results are shown in Tables 1 and 2. Chicks exposed to 10 min/hour of either bobwhite chick distress vocalizations or bobwhite chick contentment calls demonstrated a significant preference for the species-specific bobwhite maternal call over a chicken maternal call at all ages tested, p < .Ol in all cases. Analysis of latency and duration scores supported these results, with chicks showing significantly shorter latencies and longer duration in their response to the bobwhite maternal call than to the species-atypical chicken maternal call, p < .Ol in all cases.

Effects of Prenatal Auditory Stimulation

TABLE 1

329

Preference of Chicks in Simultaneous Auditory Choice Tests in Experiment 1

Preference

Bobwhite Chicken Age n Maternal Maternal No (in hours) n responding Call Call Preference

10 Min/Hour Bobwhite Distress Calls

24 ;; 20 20’ 72 I Il:* l : : 96 20 0 0

10 Min/Hour Bobwhite Contentment Calls

;; 20 20 19 17 19’ 0 1 0 2 96 20 13 1;‘: 1 1

l p -z .Ol (chi-square test).

TABLE 2 Means (and Standard Deviations) of latency and Duration Scores of Chicks

in Simultaneous Auditory Choice Tests in Experiment 1

Age (in hours)

latency Duration

Bobwhite Chicken Bobwhite Chicken Maternal Maternal Maternal Maternal

n Call Call Call Call

10 Min/Hour Bobwhite Distress Calls 24 20 31.80' 300 125.25’

72 14 (z,‘:;;! (0) (62.66) 300 122.10

(55.65) (01 (1 96 13 118.05' 281.10 y:;;!

(137.46) (58.25) (59.03)

10 Min/Hour Bobwhite Contentment Calls 24 19 43.45' 300 154.45'

(g;! (0) (;;.;g 72 17 230.50

96 13 (g;! (;;;::;I kg

(124.29) (85.72) (58.59)

'p < .Ol (Wilcoxon signed-ranks).

r:, 2.00 (6.16)

(i A.00 yg

(9:OA)

These findings stand in contrast to results of either bobwhite chick distress calls or bob- obtained from unmanipulated chicks in a previ- white chick contentment calls continued to ous experiments (Lickliter, 1994; Lickliter & demonstrate a preference for the bobwhite Virkar, 1989). Specifically, unmanipulated maternal call at 96 hours following hatching, chicks show a naive auditory preference for the indicating a deceleration in the emergence of bobwhite maternal call over a species-atypical species-typical patterns of intersensory func- maternal call at both 24 and 48 hours following tioning. It is important to note that there are hatching, but require combined maternal audi- several different types or categories of intersen- tory and maternal visual cues to direct social sory functioning, including intersensory inhibi- preferences by 72 hours following hatching. In tion and facilitation, association of multimodal this experiment, chicks exposed to 10 min/hour characteristics (multimodal coordination), and


abstraction of common information (intersensory equivalence; Botuck & Turkewitz, 1990; Turkewitz & McGuire, 1978; Turkewitz & Mellon, 1989). We are concerned only with inhibition and facilitation in this experiment.

EXPERIMENT 2

Effects of 10 Min/Hour of Prenatal

Exposure to Bobwhite Contentment Calls or Bobwhite Distress Calls on Postnatal

Auditory/Visual Responsiveness

The purpose of this experiment was to investi- gate whether the effects of prenatal exposure to bobwhite chick vocalizations generalizes to responsiveness in other sensory systems by examining the effect of these types of prenatal exposure on chicks’ postnatal visual, rather than auditory, responsiveness to maternal cues. Based on the results of Lickliter and Stoumbos ( 1991), chicks exposed to 10 min/hour of bobwhite contentment calls were expected to demonstrate a preference for species-typical maternal visual cues over species-atypical maternal visual cues by 24 hours of age. This pattern of responsiveness would indicate accelerated species-typical perceptual development. In contrast, chicks exposed to 10 min/hour of bobwhite distress calls were expected to exhibit a delay in species- typical patterns of responsiveness to maternal visual cues, indicating that type of stimulation is indeed a mediating factor in perceptual outcome.

Methods

One-hundred-twenty bobwhite quail embryo\. drawn from IS separate hatches. underwent the same procedure a\ sub-

jects in the previous experiment. Subjects were tested at tither 24 hours (II = 20 from contentment call group. and II = 20 from distress call group), 4X hours (II = 20 from COUP trntment call group), 72 hours (II = 70 from distress call group, and II = 20 from contentment call group). or 96 hour-\ (n = 20 from distress call proup) following hatching. DUI-lng the Gmultaneous-choice tests. subject\ were prcjcnted with identical species-typical auditory cues (the bobwhite matcr- nal call) paired with a stuffed model of a bobwhite hen or II stuffed model of B species-atypical scaled quail (C’ali/x~/>lo scpornata) her (see Figure I. Lickliter & Virkar. 1980). In other words, during testinp. both hen model5 emitted the same species-typical bobwhite call. requiring subject\ to direct their social preference on the basis of available static visual cues (as the identical available auditory cues did not allow a basic for decision).


The results of testing are shown in Tables 3 and 4. Chicks exposed to 10 min/hour of bob-

white distress calls did not exhibit a preference for either hen model at any age tested. Correspondingly, there were no significant differences in the subjects‘ latency and duration scores for either of the stimuli presented during testing at any age.

These findings stand in contrast to results obtained from unmanipulated chicks in prcvi- ous experiments (Lickliter, 1994; Lickliter & Virkar, 1989). In these studies, unmanipulated chicks did not demonstrate a preference for the species-typical visual cues over the species-atypical visual cues at 24 and 48 hours following hatching. but did show a preference for combined maternal auditory and maternal visual cues by 72 hours following hatching. In this experiment, chicks exposed to IO min/hour of bobwhite chick distress calls failed to demonstrate a preference for the spatially co-located bobwhite maternal auditory/ visual cues at any age tested, indicating interference with species-typical patterns of intersensory development.

In contrast. chicks exposed to 10 min/hour of bobwhite contentment calls showed a significant preference for the stuffed bobwhite hen over the species-atypical stuffed scaled quail hen by 48 hours following hatching. indicating an acceleration in species-typical visual responsiveness. Analysis of duration scores revealed that chicks showed significantly longer duration in their response to the stuffed scaled quail hen by 48 hours of age and showed significantly shorter latencies to the stuffed bobwhite hen by 72 hours of age, 17 < .05 in all cases.

These findings are similar to results obtained from a previous study in which embryos were similarly exposed prenatally to IO min/hour of bobwhite chick contentment calls (Lickliter & Stoumbos, 1991). Chicks in that experiment demonstrated a significant preference for the stuffed bobwhite hen over the stuffed scaled quail hen by 24 hours of age. In this experiment, chicks exposed to IO min/‘hour of bobwhite chick contentment calls did not exhibit this preference for the bobwhite hen until 48 hours of age. Although the results are not identical. both indicate acceleration in species-typical patterns of visual responsiveness.

Taken together. the findings from this study suggest that the type of stimulation encountered prenatally mediates the course of perceptual development. Specifically. IO min/hour of


TABLE 3

331

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

Preference

Age (in hours)

24 72 96

24

;;

Bobwhite Scaled Hen With Hen With Bobwhite Bobwhite

n Maternal Maternal No n Responding Call Call Preference

10 Mitt/Hour Bobwhite Distress Calls

20 20 10 7 20 ;: G 7 ; 20 6 3

10 Mm/Hour Bobwhite Contentment Calls

?I 18 17 5 9 : 20 16 1;: : 2

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


in Simultaneous Auditor-v-Visual Choice Tests in Exoeriment 2 r .

latency Duration

Bobwhite Scaled Bobwhite Scaled Hen With Hen With Hen With Hen With Bobwhite Bobwhite Bobwhite Bobwhite

Age Maternal Maternal Maternal Maternal (in hours) n Call Call Call Call

10 Min/Hour Bobwhite Distress Calls 24 20 112.95 136.95 94.25 67.30

72 19 1; ;;:;;I ‘1 ;;:;;I (;;:;;I m&l

96 18 (\ ;~:;;I ‘;;;:;;I W-&l ‘;;:;;I

(120.54) (116.01) (44.37) (41.76)

10 Mitt/Hour Bobwhite Contentment Calls 24 18 173.15 122.20 58.55 84.75

(\ ;;:;;I (119.04) 48 17 184.20 (;;:$1 (;;:;;I

(105.24) 72 16 126.60'

(1 ;;:;;I ‘“,g;! ‘;;:;;I

(115.92) (121.67) (54.97) (31.75)

l p -z .O5 (Wilcoxon signed-ranks).

bobwhite distress calls interferes with species- zation when the amount of stimulation is held typical perceptual development, whereas 10 constant across conditions. The question arises mitt/hour of bobwhite contentment calls accel- as to what effect a lesser amount of either dis- erates species-typical visual responsiveness. tress or contentment vocalizations might have

In sum, Experiments 1 and 2 explored how on perceptual development. For example, two distinct types of auditory stimulation pre- would 5 min/hour of prenatal exposure to bob- sented prenatally can impact perceptual organi- white contentment calls have the same impact


on postnatal auditory responsiveness as 10 min/hour of exposure to the same stimulus? Similarly, would a reduction in amount of stimulation differ depending on the type of auditory stimulation encountered? The purpose of the next two experiments was to further unpack this relationship between type of stimulation and amount of stimulation during the prenatal period.

EXPERIMENT 3


Auditory Responsiveness

Method

Subjects were 120 bobwhite quail embryos, drawn from 14 separate hatches. The shell and membrane over the air space of the egg of each subject were removed as described in the GENERAL METHODS section. After this procedure, subjects were incubated in groups of 10 to 12 same-aged embryos. All subjects were stimulated for 5 min/hour for a minimum of 24 hours from the second half of Day 21 to the second half of Day 22 of incubation. Sixty embryos were exposed to recorded bobwhite hatchling contentment vocalizations. A second group of 60 embryos were exposed to bobwhite hatchling distress vocalizations. Subjects were given a simultaneous-choice test between a bobwhite maternal call and a chicken maternal call at either 24 hours (n = 20 from contentment call group, and n = 20 from distress call group), 72 hours (n = 20 from contentment call group, and n = 20 from distress call group), or 96 hours (II = 20 from contentment call group, and n = 20 from distress call group) following hatching.


Testing results are shown in Tables 5 and 6. Chicks exposed prenatally to 5 min/hour of bobwhite chick distress calls and chicks exposed to 5 min/hour of bobwhite chick contentment calls both demonstrated a significant preference for the species-specific bobwhite maternal call over a chicken maternal call at all ages tested, p < .Ol in all cases. Analysis of latency and duration scores supported these results, with chicks showing significantly shorter latencies and longer duration in their response to the bobwhite maternal call than to the species-atypical chicken maternal call, p < .Ol in all cases. These findings indicate that 5 min/hour of prenatal exposure to either bobwhite distress calls or bobwhite contentment calls results in altered patterns of postnatal species-typical perceptual responsiveness through a continued preference for the bobwhite maternal call beyond the age when unmanipulated chicks no longer demonstrate such a preference.

Interestingly, the results from embryos exposed to only 5 min/hour of both types of prenatal auditory stimulation parallels the results from embryos exposed to 10 min/hour of the same type of prenatal auditory stimulation (Experiment l), indicating that exposing embryos to enhanced auditory stimulation of two kinds and two durations causes a prolonga- tion of responsiveness to maternal auditory cues into later stages of postnatal development.

TABLE 5 Preference of Chicks in Simultaneous Auditory Choice Tests in Experiment 3

Preference

Age (in hours)

Bobwhite Chicken n Maternal Maternal No

n responding Call Call Preference

5 Min/Hour Bobwhite Distress Calls 24

;: ?I 20

17 17 0

19 16 15’ 16’ :,

5 Min/Hour Bobwhite Contentment Calls 24

;: 18 18’

72 18 18’ : 96 20 15 13’ 1

l p < .Ol (chi-square test).


TABLE 6

333

Means (and Standard Deviations) of latency and Duration Scores of Chicks in Simultaneous Auditory Choice Tests in Experiment 3

ABe (in hours)

Latency Duration

Bobwhite Chicken Bobwhite Chicken Maternal Maternal Maternal Maternal


24 72

96

24

72

96

5 Min/Hour Bobwhite Distress Calls 17 72.90’ 274.65 123.35’ 1.50

(1 (93.58; z;:;;) (78.03) 19 242.35 (;;:g! (A&)

98.65) (l 16 111.75’ 300 9tj95)

(111.77) (0) IO)

5 Min/Hour Bobwhite Contentment Calls 18 59.55’ 300 129.10’

(i;:;;) (0) 18 (88.41; 300

(0) 15 131.25’ 266.05 3.25

(131.15) (82.96) (8.97)

l p < .Ol (Wilcoxon signed-ranks).

EXPERIMENT 4


Auditory/Visual Responsiveness

The purpose of this experiment was to assess whether the effects of 5 min/hour prenatal exposure to bobwhite chick distress calls or bobwhite chick contentment calls generalizes to responsiveness in other sensory systems by examining the effect of this exposure on chicks’ postnatal visual, rather than auditory, responsiveness to maternal cues.

Method

One hundred twenty bobwhite quail embryos, drawn from 14 separate hatches, underwent the same procedure as subjects in the previous experiment. Subjects were tested at either 24 hours (n = 20 from contentment call group, and n = 20 from distress call group), 48 hours (n = 20 from contentment call group), 72 hours (n = 20 from distress call group, and n = 20 from contentment call group), or 96 hours (n = 20 from distress call group) following hatching. During the simultaneous-choice tests, subjects were presented with identical species-typical auditory cues (the bobwhite maternal call) paired with a stuffed model of a bobwhite hen or a stuffed model of a species-atypical scaled quail hen, as in Experiment 2.


The results of testing are shown in Tables 7 and 8. Chicks exposed prenatally to 5 min/hour of

bobwhite chick distress calls did not show a preference for either hen model at any age tested. Correspondingly, there were no significant differences in the subjects’ latency and duration scores for either of the stimuli presented at any age tested. These findings indicate that 5 min/hour of prenatal exposure to bobwhite chick distress calls serves to interfere with species-typical patterns of perceptual development. Namely, these chicks fail to show a preference for species-typical maternal auditory and visual cues at the age when unmanipulated chicks exhibit this preference.

In contrast, chicks exposed prenatally to 5 min/hour of bobwhite chick contentment calls demonstrated a significant preference for the species-specific bobwhite hen over the scaled quail hen by 72 hours following hatching, p < .Ol. Analysis of latency and duration scores supported these results, with chicks showing significantly shorter latencies and longer durations in their response to the bobwhite hen than to the scaled quail hen by 72 hours of age, p < .05 in all cases. These findings parallel the pattern of visual responsiveness seen in unmanipulated chicks in previous studies in this series (Lickliter, 1994; Lickliter & Virkar, 1989), suggesting than 5 minkour of bobwhite contentment calls does not alter species-typical perceptual responsiveness.


TABLE 7 Preference of Chicks in Simultaneous Auditory-Visual Choice Tests in Experiment 4

Preference

Bobwhite Scaled Hen With Hen With Bobwhite Bobwhite

Age Maternal Maternal No (in hours) n Resp&ding Call Call Preference

5 Min/Hour Bobwhite Distress Calls

% 20 20 20 16 6 6 11 5 : 96 20 18 6 6 6

5 Min/Hour Bobwhite Contentment Calls 24

:: 19

48 17 2 i : 72 20 14 11' 2 1

l p < .Ol (A-square test)


in Simultaneous Auditory-Visual Choice Tests in Experiment 4

Age (in hours)

latency Duration

Bobwhite Scaled Bobwhite Scaled Hen With Hen With Hen With Hen With Bobwhite Bobwhite Bobwhite Bobwhite Maternal Maternal Maternal Maternal


24 72

96

24

48

72

5 Min/Hour Bobwhite Distress Calls 20 71.90 82.25 83.65

(89.74) (97.56) 16 149.25 115.50 (;~:;;I

(127.35) 18 159.30 w;' (=&I

(111.29) (117.40) (50.62)

5 Min/Hour Bobwhite Contentment Calls 19 85.75 82.35 69.35

(99.06) 17 154.55 (;;~:~;I

(59.87) 42.70

(128.50) (113.85) (50.91) 14 134.45' 219.40 56.35'

(120.88) (127.08) (56.67)

105.75 (67.96) 80.55’ ‘;;::;I

(68.74)

*p < .05 (Wilcoxon signed-ranks)

GENERAL DISCUSSlON

As illustrated in Figure 1, the results of this study demonstrate that augmented amounts of prenatal auditory stimulation can result in a developmental delay or acceleration of species- typical patterns or early perceptual development, depending on the particular type of auditory stimulation to which the embryo was exposed.

In particular, results indicate that exposure to either 10 min/hour or 5 min/hour or bobwhite chick distress calls delays species-typical patterns of postnatal intersensory responsiveness. Specifically, chicks in both of these conditions displayed a continued reliance on maternal auditory cues into late stages of postnatal development (Experiment 1 and 3) and failed to respond to maternal visual cues at ages when normally


Hours Posthatching

24 I I

48 72 96

Normal, Unstimulated Controls (Lickliter & Virkar, 1989; Lickliter, 1990b)

cl. cl. mo

10 minh Distress Calls (Experiments 1 & 2) q o q e

5 min/hr Distress Calls (Experiments 3 & 4) q eI

cl@

10 minh Contentment Calls (Experiments 1 & 2)

10 minh Contentment Calls (Stoumbos & Lickliter, 1991)

5 min/hr Contentment Calls (Experiments 3 & 4) 4

335

WO

El.

Cl.

cl

Figure 1. Summa 7c

of the postnatal preferences of bobwhite chicks for maternal auditory and visual cues fo owing normal or augmented prenatal auditory experience.

reared chicks exhibit this species-specific ability (Experiment 2 and 4). In contrast, prenatal exposure to 10 min/hour of bobwhite contentment calls resulted in a continued preference for maternal auditory cues into late stages of development (Experiment 1) and an acceleration in preferential responsiveness to maternal visual cues (Experiment 2). Chicks exposed to only 5 min/hour of bobwhite contentment calls demonstrated a continued preference for maternal auditory cues into late stages of postnatal development (Experiment 3) and exhibited species-typical responsiveness to maternal visual cues (Experiment 4). In sum, the findings indi-

cate that exposure to augmented amounts of prenatal auditory stimulation does not, in and of itself, interfere with postnatal perceptual functioning. Rather, the amount of auditory stimulation and the type of auditory stimulation interact to determine subsequent perceptual functioning. In fact, type of auditory stimulation appears to be a more influential factor than amount of stimulation in affecting perceptual development.

Interestingly, in all conditions in this study, chicks exposed to enhanced prenatal auditory stimulation continued to respond to maternal auditory cues beyond the age when unmanipulated chicks no longer respond to auditory cues.


These results are consistent with a previous experiment in this series which demonstrated that bobwhite quail chicks exposed to particular auditory stimulation during the prenatal period prefer postnatal testing stimuli that match their prior experience (McBride & Lickliter, 1995). In addition, chicks in that experiment displayed a postnatal preference for familiar types of auditory stimuli over familiar amounts of sensory stimuli (McBride & Lickliter, 1995). Taken together, these results indicate the existence of a hierarchical relationship between these two features of sensory stimulation. Specifically, the type of stimulation is a more influential feature of sensory stimulation than is amount of stimulation, at least within the auditory modality.

Results from previous experiments with bobwhite chicks support this notion that the type of stimulation encountered is a crucial factor in perceptual development. For example, Lickliter and Stoumbos (1991) demonstrated that increased prenatal amounts of bobwhite contentment calls accelerate postnatal visual responsiveness to maternal cues, whereas increased prenatal amounts of bobwhite contentment calls with a faster than normal repetition rate do not result in this acceleration. In a similar vein, McBride and Lickliter (1994) found that chicks exposed to bobwhite distress calls during early postnatal development exhibit species-atypical patterns of perceptual development. In contrast, chicks exposed to bobwhite contentment calls during early postnatal development exhibit species-typical patterns of perceptual development.

Although the type of stimulation available to the developing embryo or neonate has emerged as an important variable in perceptual development, the amount of sensory stimulation should not be undercharacterized as an important factor in species-typical perceptual development. As suggested by Radell and Gottlieb (1992) sensory stimulation that falls within some “optimal” range appears to maintain or facilitate normal patterns of perceptual functioning (Lickliter, 1990a, 1990b; Lickliter & Stoumbos, 1991; Radell & Gottlieb, 1992). On the other hand, substantially attenuated or substantially increased amounts of stimulation appear to interfere with both the emergence of species-typical patterns of intersensory functioning (Gottlieb, 1993; Lickliter & Lewkowicz. 1995: Sleigh &

Lickliter, 1995) and prenatal auditory learning (Gottlieb et al., 1989; Lickliter & Hellewell, 1992; Lickliter & Lewkowicz, 1995; Radell & Gottlieb, 1992; Sleigh & Lickliter, 1995). In light of these experiments, the amount of stimulation that is considered within an organism’s optimal range may be dependent upon the particular type of sensory stimulation that is being encountered. For example, both 5 mimhour and 10 min/hour of bobwhite distress calls result in a delay of species-typical perceptual responsiveness, whereas 5 mm/hour and 10 mitt/hour of bobwhite contentment calls maintain or accelerate species-typical perceptual responsiveness. These results support the idea that the emergence of species-typical perception is a proba- bilistic phenomenon, rather than merely the unfolding of a predetermined substrate (Gottlieb, 197 1). Future studies should examine the impact of prenatal exposure to substantially increased amounts of bobwhite contentment calls on subsequent postnatal perceptual development to determine if greatly augmented amounts of this type of stimulation can result in altered species- typical intermodal responsiveness.

Future studies should also address the specific features of sensory stimulation that mediate patterns of perceptual responsiveness. For example, previous work has demonstrated that precocial avian embryos are sensitive to repetition rates (notes per second) of auditory stimulation (Gottlieb, 1981; Miller, 1983). Miller (1983) manipulated the repetition rates of a mallard duckling call and demonstrated that slow repetition rates were associated with behavioral inhibition in mallard ducklings, whereas faster repetition rates were associated with behavioral excitation. These findings suggest that repetition rates may mediate arousal levels in the young organism and impact subsequent perceptual responsiveness. In this light. McBride and Lickliter (1994) recently provided an acoustical analysis of the bobwhite contentment call and the bobwhite distress call, which revealed that the bobwhite distress call has a higher repetition rate than the bobwhite contentment call. Thus, the behavior patterns of birds in this experiment may have been the result of the unique repetition rates of the two types of auditory stimulation employed. Future studies should manipulate the repetition rates of these species-specific calls in order to assess whether particular repetition rates reliably asso-

Effects of Prenatal Auditory Stimulation 337

ciated with particular behavioral states and arousal levels.

This study focused on the effects of altering the nature of the embryo’s typically structured developmental context; what remains to be explored are the organismic aspects of the relationship between amount and type of stimulation experienced and subsequent perceptual behavior patterns. For example, the specific mechanisms that mediate the alteration of intersensory functioning following specific prenatal auditory stimulation is presently unknown. It is possible that the types and amounts of stimulation typically encountered during the prenatal period serve to maintain the embryo’s overall level of arousal in a range that is optimal for attending and responding to sensory stimulation. Deviations either above or below this optimal range apparently negatively impact the young organisms’ ability to attend to available sensory stimulation, at least during the perinatal period (Lickliter & Lewkowicz, 1995; Radell & Gottlieb, 1992). Changing either the type or amount of stimulation may serve to shift the young organisms’ arousal level either above or below this optimal range. Based on his work with domestic chicks, Gray (1990) argued that responsiveness to experimental manipulations is mediated by the arousal level of the organism. Excessive or reduced arousal levels are generally associated with poor performance, whereas a moderate level of arousal is associated with peak performance. In other words, the amount of external stimulation may impact an organism’s arousal level and thereby serve to increase or decrease the embryo’s sensitivity to specific sensory stimulation present in the perinatal environment.

Efforts towards uncovering how the arousal level of the organism may alter sensitivity to specific sensory inputs have been provided by work with human infants. For example, Lewkowicz and Turkewitz (1980) demonstrated that prestimulating an infant with a pulse of white noise resulted in infants’ increased looking at a dimmer light and decreased looking at a brighter light in comparison to unstimulated infants. In a subsequent experiment, infants exposed to auditory stimulation immediately preceding or presented concurrently with visual stimuli preferred the less intense visual stimulation (Lewkowicz & Turkewitz, 1981). Similar results were found by Gardner, Lewkowicz,

Rose, and Karmel (1986) using either auditory or visual stimulation prior to testing. Taken together, these findings suggest that changing the arousal level of infants through visual or auditory prestimulation can alter their subsequent visual stimulation preference and empha- size that intersensory development is context sensitive. That is, emerging intersensory capac- ities can be strongly influenced or modified by specific features of the infant’s surround. As demonstrated in our study, local variability can facilitate or interfere with the infant’s intersensory performance.

The idea that control for any developmental outcome resides in the structure and nature of the relationships within and between internal and external variables (rather than in any individual factor) is not widely appreciated but clearly has important implications for the study of early perceptual organization. In particular, the notions of diffuse control and reciprocal interaction highlight the need for an explicit empirical concern with the dynamic relationship between the developing organism and its structured environment. This larger focus clearly stands in contrast to the more limited tradi- tional focus of describing the infant and its emerging intersensory capabilities independent of specific sensory stimulation or context.

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01 August 1995; Revised 19 February 1996 n

type and amount of prenatal stimulation alters perceptual responsiveness in bobwhite quail chicks

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