Developmetal Psychology 9, Vol. 31. No. 4, 9-18 Copyright 9 by the America Psychological Associatio, Ic. OI2-149/9/S3.OO Itersesory Experiece ad Early Perceptual Developmet: Atteuated Preatal Sesory Stimulatio Affects Postatal Auditory ad Visual Resposiveess i Bobwhite Quail Chicks {Colius virgiiaus) Robert Lickliter Virgiia Polytechic Istitute ad State Uiversity David J. Lewkowicz New "fork State Istitute for Basic Research i Developmetal Disabilities Related experimets examied the effects of atteuated preatal sesory stimulatio o subsequet postatal auditory ad visual resposiveess i precocial bobwhite quail chicks {Colius virgiiaus). Results revealed that deyig quail embryos the preatal vestibular ad tactile stimulatio provided by broodmates durig icubatio alters pre- ad postatal perceptual fuctioig. Chicks icubated i physical isolatio durig the late stages of preatal developmet respoded to materal auditory cues ito later stages of the postatal period ad failed to respod to materal visual cues at ages commually icubated chicks typically display such visual resposiveess. I additio, embryos icubated i physical isolatio failed to exhibit early auditory learig of a idividual materal call, a behavior reliably see i commually icubated embryos. Take together, these results ad those from related studies idicate that a substatial decrease or icrease i the rage of sesory stimulatio ormally preset i the preatal period ca result i a slowig of the rate of speciesspecific perceptual developmet ad suggest that some optimal rage of preatal sesory stimulatio is ecessary for species-typical perceptual capacities to emerge. The preatal eviromet of avia ad mammalia species is rich i tactile, vestibular, chemical, ad auditory sesory stimulatio (Freema & Vice, 74; Roca, Lamki, & Alberts, 93; Smotherma & Robiso, 8). I may species, the sesory systems capable of respodig to these types of iputs are already well developed ad fuctioal before birth or hatchig (Alberts, 84; Bradley & Mistretta, 7; Gottlieb, 71). The availability of a rich sesory eviromet durig the preatal period, coupled with the embryo or fetus's capacity to respod to it, suggests that the developmet of early perceptual orgaizatio may be strogly iflueced by preatal sesory experiece. I this light, several studies have show that the huma fetus is sesitive ad resposive to auditory stimulatio ad ca retai the effects of preatal auditory experiece ito postatal life (DeCasper & Spece, 91; Fifer & Moo, 88). Studies with both ifrahuma mammalia species ad huma fetuses have also show that preatal experiece with chemosesory stimulatio ca exert sigificat effects o subsequet postatal behavior. For example, Smotherma ad Robert Lickliter, Departmet of Psychology, Virgiia Polytechic Istitute ad State Uiversity; David J. Lewkowicz, New %rk State Istitute for Basic Research i Developmetal Disabilities, State Islad, New York. This research was supported i part by Grat MH48949 from the Natioal Istitute of Metal Health. We followed both atioal ad istitutioal guidelies for the care ad use of aimal subjects. We thak Robi Paeto Cooper for her costructive commets o the mauscript ad Thomas McBride for assistace with data collectio. Correspodece cocerig this article should be addressed to Robert Lickliter, Departmet of Psychology, Virgiia Polytechic Istitute ad State Uiversity, Blacksburg, Virgiia 241-43. Robiso (87) demostrated that rat fetuses exhibit a form of olfactory sesitizatio that has log-lastig effects o postatal sucklig ad cosummatory behaviors. Marlier, Schaal, ad Soussiga (94) showed that huma eoates prefer the smell of amiotic fluid over distilled water, suggestig that experiece with the preatal chemical eviromet has cosequeces for the postatal fuctioal orgaizatio of the olfactory system. A potetially importat feature of preatal sesory experiece is that it ca be multisesory i ature. That is, a mammalia fetus or avia embryo may experiece sesory stimulatio of the vestibular, somesthetic, chemical, or auditory modalities simultaeously or sequetially. This coditio raises the iterestig possibility that preatal stimulative effects i oe sesory modality may have lastig effects o resposiveess to stimulatio i other modalities. Recet work with a variety of aimal species has demostrated such effects of modified periatal sesory experiece i oe modality o subsequet postatal perceptual orgaizatio (Baker & Lickliter, 93; Forema & Altaha, 91; Gottlieb, 93; Gottlieb, Tomliso, & Radell, 89; Key & Turkewitz, 8; Lickliter, 9a, 9b, 94; Lickliter & Stoumbos, 91; Radell & Gottlieb, 92; Symos & Tees, 9) ad has raised a umber of questios regardig the particular aspects of periatal sesory stimulatio that ca mediate chage i early itersesory relatioships. For example, several recet studies usig aimal embryos ad ifats have demostrated that specific experietial maipulatios of periatal sesory stimulatio ca either result i the facilitatio of early itersesory resposiveess (Lickliter, 9a, 94; Symos & Tees, 9) or iterfere with early itersesory capacities (Key & Turkewitz, 8; McBride & Lickliter, 94). What remais uclear at preset is why sesory augmetatio or deprivatio procedures ca result i the facilitatio of itersesory itegratio i some studies ad disruptive effects o itersesory itegratio i others. 9
1 ROBERT LICKLITER AND DAVID J. LEWKOWICZ Although the effects that altered periatal sesory experiece may have o subsequet perceptual orgaizatio is likely to deped o a umber of ested factors, icludig the timig of the maipulatio i relatio to the developmetal stage of the ifat (Gottlieb, 71; Turkewitz & Key, 82) ad the type of stimulatio provided or deied (Gottlieb, 81,91a;McBride&Lickliter, 94), several recet studies usig precocial birds have also idicated that the overall amout of sesory stimulatio preset i the periatal eviromet ca have a sigificat ifluece o the embryo or eoate's sesitivity to specific sesory iput (Gottlieb, 91b, 93; Gray, 9; McBride & Lickliter, 93). I particular, these studies suggest that the amout of sesory stimulatio provided by social experiece with broodmates i the period immediately followig hatchig ca affect the arousal level of hatchligs ad thereby serve to either icrease (Gottlieb, 93; McBride & Lickliter, 93) or decrease (McBride & Lickliter, 94) chicks' sesitivity to specific auditory or visual stimulatio preset i the postatal eviromet. For example, a recet study usig duckligs (Gottlieb, 93) foud that tactile stimulatio afforded by ormal social iteractio with broodmates is essetial for postatal auditory learig of a omateral call; duckligs reared i tactile isolatio from cospecifics did ot exhibit the usual postatal auditory-learig abilities see i group-reared birds. Gottlieb (93) reasoed that tactile isolatio deprives hatchligs of ormal levels of periatal sesory stimulatio ad thereby egeders a high level of arousal i hatchligs. This high level of arousal (assessed by umber of distress vocalizatios emitted by subjects) appears to disrupt the youg ducklig's attetioal capacity for the experimetal auditory stimulus ad thus serves to iterfere with typical patters of early auditory learig. To further examie this otio of optimal levels or thresholds of sesory stimulatio as it applies to the preatal period of developmet, we desiged the preset study to determie whether atteuatig the amout of sesory stimulatio ormally preset i the preatal eviromet would affect subsequet perceptual fuctioig i bobwhite quail chicks. Specifically, i light of previous research with precocial avia hatchligs (see Lickliter, Dyer, & McBride, 93, for a review), we predicted that avia embryos deied the ormally occurrig vestibular ad tactile stimulatio typically provided to them by broodmates durig the late stages of the preatal period would likely demostrate patters of perceptual orgaizatio differet from embryos allowed urestricted physical stimulatio from their broodmates. Specifically, we reasoed that because of their substatially reduced levels of ormally occurrig preatal sesory stimulatio, embryos icubated i physical isolatio from cospecifics would show fuctioal deficits i their subsequet auditory ad visual resposiveess to species-specific materal cues. Geeral Method Certai features of our experimetal desig were commo to all experimets, so we describe these first before presetig the particular details of each experimet. Subjects Three hudred ad sixty-oe icubator-reared bobwhite quail chicks (Colius virgiiaus) were used as subjects. Fertile, uicubated eggs were received weekly from a commercial supplier ad were set i a Petersime Model I icubator, maitaied at 37. C ad 8%-9% relative humidity. After 2 days of icubatio, the eggs were trasferred to a hatchig tray located at the bottom of the icubator. To cotrol for possible effects of variatios i developmetal age, oly those birds that hatched betwee the last half of day 22 ad the first half of day 23 of icubatio were used as subjects. Chicks that hatched earlier or later tha this 24-hr widow were excluded from the various experimets. The embryo's age is calculated o the basis of thefirstday of icubatio beig day, the secod 24-hr of icubatio beig day 1, ad so o. This restrictio i developmetal age cosistetly excluded approximately 2% of the chicks from ay give batch (week) of eggs. The possible ifluece of betwee-batches variatio i behavior was cotrolled by drawig subjects for each experimetal group from three or more differet batches (i.e., weeks) of eggs. As a result of their icubator rearig, the oly souds to which embryos ad hatchligs were exposed util the time of experimetal maipulatio or testig were their ow embryoic ad postatal vocalizatios (ad those of their broodmates) ad the low-frequecy backgroud oises emaatig from the icubator fa ad motor. Followig hatchig, subjects were group-reared i large plastic tubs (4 X 2 X 1 cm) cotaiig 1-12 same-age chicks to mimic aturally occurrig brood coditios (Stokes, 7). The soud-atteuated room i which the hatchligs were kept was illumiated by a 1-W brooder lamp suspeded above the plastic rearig tubs, which maitaied a ambiet air temperature of approximately 3 C. Food ad water were cotiuously available throughout the duratio of each experimet. Procedure To esure that the embryos could hear or see the sesory stimulatio preseted i the various experimets i the period before hatchig, durig the secod half of the 21st day of icubatio, we removed a portio (approximately 1. cm i diameter) of the shell ad ier-shell membrae over the air space of the egg of each subject. The embryo's bill usually peetrates the air space at the large ed of the egg early o day 21, ad at this time the embryo begis to respire ad vocalize (Freema & Vice, 74). As a result, removig the top portio of the shell (the embryo's postural orietatio is ot altered ad the head ad body remai cofied i the shell) does ot affect icubatio, survivability, or species-typical perceptual behavior (Lickliter, 9b; Lickliter & Stoumbos, 91). Followig the egg-opeig procedure, each embryo (still cofied withi its egg) was placed i a idividual, opaque plastic tub (7 cm 3 ) ad was icubated i a portable icubator for the last 24-3 hr of icubatio. Each portable icubator cotaied 12 of these isolatio tubs; embryos were thus able to hear but ot physically cotact other broodmates durig the late stages of icubatio. Temperature ad humidity were maitaied as durig earlier icubatio. Testig Testig took place 24, 48, or 72 hr (±3 hr) after hatchig. Each chick was tested oly oce. The testig apparatus was located i a soudatteuated room ad cosisted of a large circular area, 1 cm i diameter, surrouded by a black curtai that shielded the observer from the subject's view. The walls of the apparatus were lied with foam to atteuate echoes, ad the floor was paited flat black. Two rectagular approach areas (32 X 1 cm) were delieated o opposite sides of the area by gree lies paited o thefloor.these approach areas costituted less tha % of the total area of the area, so preferece scores were based o strict criteria. To begi a preferece test, we placed each chick at a start poit equidistat from the two approach areas. A midrage dome-radiator speaker was positioed behid the curtai i each of the approach areas, ad each speaker was coected to its ow cassette tape player located at a cotrol table. A observer who was uaware of each experimet's desig sat at this table ad observed each
INTERSENSORY EXPERIENCE AND PERCEPTUAL DEVELOPMENT 11 chick's activity through a large mirror positioed above the area. The testig room were maitaied at approximately 2 C throughout the study. All of the birds were tested idividually i a -mi simultaeous choice test ad were scored o both the latecy of approach ad duratio of time spet i each of the two approach areas. Depedig o the particular experimet, each chick was tested for its preferece betwee either two auditory stimuli or two audiovisual stimuli preseted o either side of the area. The locatio of the auditory ad visual stimuli preseted durig testig i each experimet was alterated betwee chicks to prevet ay possible side bias from ifluecig results. Latecy was scored as the amout of time (i secods) elapsed from the oset of the trial util the subject etered a approach area. Duratio was scored as the cumulative amout of time (i secods) the bird remaied i a approach area durig the -mi test. Whe, over the course of the -mi trial, a chick stayed i oe approach area for more tha twice the time it spet i the opposig approach area, a preferece for that stimulus was recorded. Occasioally, a bird etered both approach areas durig a test without showig a preferece for either oe. This behavior was scored as "No preferece" i the tables showig test results. The subject had to remai i a approach area for at least 1 cosecutive secods for a duratio score to be couted; this criterio preveted ay radom movemets from beig couted as a respose to the preseted stimuli. If a subject did ot move from the start poit durig the test trial, it was cosidered a orespoder ad received a score of 3 s for latecy (the legth of the trial) ad s for duratio for both test stimuli. Data Aalysis The primary data of iterest i each experimet were the measures of preferece (derived from latecy ad duratio of respose) for the auditory ad visual stimuli preseted durig the trials. Two such measures of preferece were used: (a) Differeces i the latecy of approach to each stimulus by a subject i a group was evaluated by the Wilcoxo matched-pairs siged-raks test, ad (b) a idividual preferece, derived from duratio of time spet i proximity to each stimulus, was assiged to ay subject that stayed i oe area for more tha twice as log as the other; this measure was evaluated by the chi-square test. Prelimiary aalyses of these two measures idicated that they were perfectly correlated, so to reduce redudacy, we did ot preset latecy measures i ay detail. Sigificace levels set at p <. were used to evaluate results, ad all reported p values are two-tailed. Experimet 1: Effects of Atteuated Preatal Sesory Stimulatio o Postatal Auditory Resposiveess Previous studies have demostrated that at 24 hr ad 48 hr followig hatchig, bobwhite quail chicks ca direct their social prefereces solely o the basis of available materal auditory cues (Heato, Miller, & Goodwi, 78; Lickliter, 94; Lickliter & Virkar, 89). By 72 hr of age, chicks require combied materal auditory ad visual stimulatio to direct their social prefereces (Lickliter & Virkar, 89; McBride & Lickliter, 94). I cotrast, chicks exposed to uusually early visual experiece as embryos do ot exhibit a preferece for the bobwhite materal call at either 24 hr or 48 hr followig hatchig (Lickliter, 9b). Rather, these chicks require both materal auditory ad visual cues to direct their preferetial resposiveess by 24 hr followig hatchig (Lickliter, 9a, 9b). This fidig suggests that augmeted preatal visual stimulatio serves to accelerate the developmetal emergece of itersesory itegratio that uder ormal circumstaces does ot appear util 72 hr followig hatchig (see Lickliter & Baker, 94, for a more detailed discussio). The specific mechaism that mediates the acceleratio of itersesory itegratio followig uusually early visual experiece is presetly ukow. However, the uusually early visual stimulatio preseted to embryos i the Lickliter (9a, 9b) studies was give to commually icubated embryos. As a result, these embryos were exposed to a variety of sesory stimuli from broodmates i additio to preatal visual stimulatio. These various stimuli icluded the vestibular ad tactile stimulatio provided by broodmates durig the hatchig process as emergig hatchligs roll ito, push agaist, ad climb over other eggs of their clutch. It is possible that this "backgroud" sesory stimulatio provided by broodmates durig the late stages of icubatio is essetial i maitaiig the embryos' overall level of arousal i a rage that is optimal for attedig ad respodig to the premature visual stimulatio. As a first step i examiig this possibility, i the preset experimet, we deprived oe group of bobwhite embryos of ormally occurrig physical cotact with broodmates durig the last stages of icubatio to determie whether the absece of such sesory experiece plays a role i their subsequet perceptual fuctioig. A secod group of bobwhite embryos was also deprived of ormally occurrig vestibular ad tactile stimulatio from broodmates ad i additio received visual stimulatio before hatchig. If the backgroud level of stimulatio provided by physical cotact with broodmates is essetial to the facilitatio of embryos' resposiveess to earlier-tha-usual visual iput, the embryos deprived of such stimulatio should exhibit patters of resposiveess differet from those previously observed i commually icubated chicks. Method Oe hudred ad twety bobwhite quail chicks, draw from 11 separate hatches, served as subjects. Subjects were divided ito a isolatio group («= 4) ad a isolatio-visual stimulatio group ( = ). Chicks i the isolatio group uderwet the egg-opeig procedure o the secod half of day 21, as described i the Geeral Method sectio, ad were the icubated to hatchig i isolatio tubs placed i a group of 12 i a portable icubator located i a darkeed room. These subjects received atteuated sesory stimulatio from broodmates durig the last 24-3 hr before hatchig, i that they could hear other embryos i the icubator but could ot physically cotact these embryos. Because of their lack of physical cotact with broodmates, embryos were deied the vestibular ad tactile stimulatio typically provided to them by broodmates durig the hatchig process. Chicks i the isolatio-visual stimulatio group uderwet the same egg-opeig procedure ad were the icubated to hatchig i isolatio tubs while beig exposed to a 1-W light pulsed at 3 cycles per secod (maximum flash eergy = 4-W s) for 1 mi each hour. This temporally pattered light was located immediately above the Plexiglas top of the icubator, ad particular care was take to esure that the presece of the light did ot alter the ambiet air temperature or relative humidity withi the icubator. Embryos i this group thus received atteuated sesory stimulatio from broodmates ad uusually early visual stimulatio for 1 mi each hour durig the last 24 to 3 hr before hatchig. Although the precocial avia embryo is resposive to preatal visual stimulatio (Heato, 73; Oppeheim, 8), the embryo does ot ordiarily experiece pattered visual stimulatio util after hatchig from the egg. Followig hatchig, all chicks from both groups were reared socially i groups of 1-12 same-age chicks, i which they remaied util testig at
12 ROBERT LICKLITER AND DAVID J. LEWKOWICZ 24,48, or 72 hr of postatal age. Testig cosisted of presetig subjects with a simultaeous choice test betwee the bobwhite materal call ad a chicke materal call (see Heato et al., 78, for acoustical details). Choice, latecy, ad duratio of respose were scored as described i the Geeral Method sectio. Results ad Discussio The results of this experimet are illustrated i Table 1. Birds i both the isolatio group ad the isolatio-visual stimulatio group exhibited a sigificat preferece for the bobwhite materal call over the chicke materal call at 24, 48, ad 72 hr followig hatchig (p <.1). The aalysis of the latecy scores further supported these fidigs: At all ages tested, both groups showed shorter latecies i their respose to the bobwhite materal call over the chicke materal call (p <.1). These fidigs stad i cotrast to the results obtaied from commually icubated chicks i previous studies (Baker & Lickliter, 93; Lickliter, 9a, 9b, 94; Lickliter & Virkar, 89). I these studies, ormally reared chicks cosistetly preferred the bobwhite materal call over the chicke materal call at 24 hr ad 48 hr followig hatchig, but ot at 72 hr. I additio, commually icubated chicks who received uusually early (preatal) visual experiece as embryos did ot prefer the bobwhite materal call preseted without materal visual cues at 24, 48, or 72 hr followig hatchig (Lickliter, 9a, 9b). I the preset experimet, chicks icubated i isolatio (isolatio group) ad chicks icubated i isolatio ad exposed to uusually early visual experiece (isolatio-visual stimulatio group) demostrated a auditory preferece for the bobwhite materal call ito later stages of postatal developmet tha see i commually icubated chicks. Specifically, chicks i both groups cotiued to respod preferetially to the bobwhite materal call through 72 hr of age, whether or ot they had received uusually early visual stimulatio as embryos. The fact that chicks icubated i isolatio ad exposed to preatal visual experiece cotiued to respod to materal auditory cues at 72 hr is particularly strikig, i that these chicks respoded to the materal call some 3 days later ito postatal developmet tha commually icubated chicks receivig preatal visual stimulatio (Lickliter, 9a). It appears that elimiatio of the ormally available sesory stimulatio were from broodmates durig the late stages of icubatio alters the embryo's sesitivity to the presetatio of preatal visual stimulatio, i that chicks receivig uusually early visual experiece showed the same patter of resposiveess to the materal call as chicks ot receivig visual experiece as embryos (Table 1). What is ot clear from the preset results, however, is how geeral this effect is. If the sesory stimulatio provided by broodmates uder ormal icubatio coditios serves to provide a level of stimulatio ecessary for respodig to uusually early visual stimulatio, the the effects foud i the preset experimet should geeralize to resposiveess i other sesory systems. The purpose of the ext experimet was to ivestigate this possibility by assessig the effects of isolatio ad preatal visual stimulatio o chicks' postatal visual, rather tha auditory, resposiveess to materal cues. Experimet 2: Effects of Atteuated Preatal Sesory Stimulatio o Postatal Visual Resposiveess Previous research has revealed that ormally reared, commually icubated bobwhite quail chicks show a sigificat visual preferece for a bobwhite he model over a scaled quail he model whe botl} are emittig the same bobwhite materal call by 72 hr followig hatchig (but ot at earlier ages; Lickliter, 94; Lickliter & Virkar, 89; McBride & Lickliter, 93). I cotrast, commually icubated chicks who received preatal visual experiece as embryos demostrate a preferece for the bobwhite he over the scaled quail he (whe both are emittig the same bobwhite materal call) by 24 hr followig hatchig (Lickliter, 9a). It is importat to ote that the static visual cues provided by the he models aloe are ot sufficiet to elicit preferetial resposiveess at ay of the ages tested. Rather, materal visual cues must be preseted with the materal call to be effective i directig social prefereces (Lickliter, 94; Lickliter & Virkar, 89). The preset experimet was desiged to examie the ifluece of preatal sesory stimulatio from broodmates o chicks' postatal visual resposiveess to materal cues. If the Table 1 Preferece of Chicks i Simultaeous Auditory Choice Tests i Experimet 1 Preferece Group/age respodig Bobwhite materal call Chicke materal call No preferece Isolatio 24 hr 48 hr 72 hr Isolatio-visual stimulatio 24 hr 48 hr 72 hr 23 22 18 18 1 1 14 14 * 18* 1* 14* 13* 14* 1 1 * p <.1 (chi-square test).
INTERSENSORY EXPERIENCE AND PERCEPTUAL DEVELOPMENT 13 lack of ormally preset sesory stimulatio from broodmates makes it more difficult for embryos to atted or respod to uusually early visual stimulatio, the chicks icubated i physical isolatio from broodmates should ot demostrate the postatal acceleratio of the emergece of itersesory itegratio previously observed i commually icubated chicks exposed to preatal visual stimulatio durig the late stages of icubatio. Method A total of 141 bobwhite quail chicks, draw from 1 separate hatches, served as subjects. Experimetal chicks were divided ito a isolatio group ( = 2) ad a isolatio-visual stimulatio group («= 9) ad received the same preatal procedures as subjects i the previous experimet. Cotrol chicks ( = 2) were commually icubated ad received the same preatal visual stimulatio described i Experimet t. Followig hatchig, all chicks were reared socially i groups of 1-12 same-age chicks ad were tested idividually at 24,48, or 72 hr of postatal age. Testig cosisted of presetig hatchligs with a simultaeous choice test betwee the bobwhite materal call paired with either a stuffed adult bobwhite he or a stuffed scaled quail he (for a photo of these stimuli, see Baker & Lickliter, 93, Figure 1). I other words, durig testig, both he models were emittig the same species-typical bobwhite materal call, requirig subjects to direct their social preferece o the basis of available visual cues. Choice, latecy, ad duratio of respose were scored as described i the Geeral Method sectio. Results ad Discussio The results of testig are show i Table 2. Experimetal chicks i both the isolatio group ad the isolatio-visual stimulatio group did ot show a preferece for either the bobwhite he model paired with the bobwhite materal call or the scaled quail he model paired with the bobwhite materal call at ay of the ages tested. Correspodigly, there were o sigificat differeces i latecy scores for either stimulus array i either experimetal group at 24,48, or 72 hr followig hatchig. These results differ markedly from the results obtaied from the commually icubated ad visually stimulated cotrol chicks, which preferred the bobwhite he over the scaled quail he by 24 hr followig hatchig (see Table 2; see also Lickliter, 9a). I additio, the results from experimetal chicks i this study differed from the results of commually icubated chicks i previous studies, which did ot receive uusually early visual stimulatio (Baker & Lickliter, 93; Lickliter, 9a, 9b; Lickliter & Virkar, 89; McBride & Lickliter, 93). I these studies, ormally reared, umaipulated chicks cosistetly preferred the bobwhite he paired with the bobwhite materal call over the scaled quail he paired with the bobwhite materal call by 72 hr followig hatchig. I the preset experimet, chicks icubated i isolatio (isolatio group) ad chicks icubated i isolatio ad exposed to uusually early visual experiece (isolatio-visual stimulatio group) did ot prefer the bobwhite he by 72 hr of age, idicatig that the oset of chicks' visual resposiveess to materal cues is compromised as a result of atteuated preatal stimulatio. These fidigs further support the otio that physical isolatio from broodmates somehow alters the embryo's sesitivity to the augmeted visual stimulatio preset i the period before hatchig. If this patter is geeralizable to other modalities, the embryos' sesitivity to augmeted auditory stimulatio should also be adversely affected uder coditios of atteuated preatal sesory stimulatio. The purpose of the ext experimet was to examie this possibility. Experimet 3: Effects of Atteuated Preatal Sesory Stimulatio o Auditory Learig Previous research has show that commually icubated bobwhite quail embryos ca lear a idividual bobwhite materal call ad remember that familiar call for at least 24 hr after exposure. Specifically, embryos exposed to a particular variat of the bobwhite materal call durig the later stages of icubatio subsequetly demostrate a auditory preferece for that call over aother bobwhite materal call whe tested postatally (Lickliter & Hellewell, 92). To further ivestigate the impact of preatal stimulatio from broodmates o early perceptual fuctioig, this experimet assessed auditory learig i Table 2 Preferece of Chicks i Simultaeous Auditory- Visual Choice Tests i Experimet 2 Preferece Group/age respodig Bobwhite call & bobwhite he Bobwhite call & scaled he No preferece Isolatio-o stimulatio 24 hr 48 hr 72 hr Isolatio-visual stimulatio 24 hr 48 hr 72 hr Commual-visual stimulatio (cotrols) 24 hr 2 21 21 2 21 18 2 17 1 1 1 13 17 9 4 8 13* 8 7 3 2 2 2 4 7 2 * p <.1 (chi-square test).
14 ROBERT LICKLITER AND DAVID J. LEWKOWICZ bobwhite embryos deied physical cotact with broodmates durig the later stages of icubatio. Method Sixty bobwhite quail embryos, draw from seve separate hatches, served as subjects. The embryos were divided ito a cotrol group ( = 2), a isolatio-o-exposure group ( = 2), ad a isolatioexposure group ( = 2). Experimetal embryos i the isolatio-oexposure group uderwet the egg-opeig procedure as i the previous experimets ad were the icubated to hatchig i isolatio tubs i a portable icubator located i a darkeed room. Experimetal embryos i the isolatio-exposure group uderwet the egg-opeig procedure ad were the icubated i isolatio tubs i a darkeed room while beig exposed to a idividual bobwhite materal call (Call B) for 1 mi each hour for 24 hr before hatchig. Cotrol embryos uderwet the egg-opeig procedure ad were the commually icubated i a darkeed room while beig exposed to bobwhite materal Call B. Auditory stimulatio commeced o the secod half of the 21st day of icubatio ad cotiued through the secod half of the 22d day of icubatio. Total preatal auditory stimulatio with the materal call thus amouted to approximately 4 hr for the isolatio-exposure group ad the commual cotrol group. The recordig of the idividual materal call was played to the embryos through a Maratz Model PMD 221 cassette recorder ad preseted at a peak itesity of db, as measured by a Bruel & Kjaer Model 2232 soud-level meter. All the ormally occurrig acoustic compoets of the materal vocalizatio were preset ad ualtered. After hatchig, all subjects were reared socially with 1 to 12 same-age chicks util testig at 24 hr of postatal age. Durig testig, idividual subjects were give a simultaeous choice test betwee the familiar bobwhite materal call (Call B) ad a ufamiliar variat of the bobwhite materal call (Call A). These two materal calls were recorded i thefieldad were similar i phrasig, call duratio, repetitio rate, domiat frequecy, ad frequecy modulatio (see Table 1 i Heato et al., 78). The soud itesity of both of the calls peaked at db at the poit i which the chick was itroduced ito the test area. Choice, latecy, ad duratio of respose was scored as described i the Geeral Method sectio. Results ad Discussio As show i Table 3, the two variats of the bobwhite materal call were equally attractive to the isolatio-o-exposure chicks at 24 hr followig hatchig. Birds which demostrated a preferece from this group (i.e., spet twice as log i oe approach area as the other) were just as likely to prefer Call A (the ufamiliar call) as Call B (the familiar call) i the simultaeous choice test. Aalysis of the latecy of respose also revealed o preferece betwee the two bobwhite materal calls. Experimetal chicks exposed to Call B as isolated embryos (isolatio-exposure group) likewise did ot demostrate a preferece for either of the two materal calls at 24 hr followig hatchig. The aalysis of latecy scores by the Wilcoxo test further supported this fidig: Scores were ot sigificatly differet betwee the familiar ad ufamiliar auditory stimuli preseted durig testig. I cotrast, commually icubated chicks i the cotrol group demostrated a sigificat preferece for the familiar materal Call B at 24 hr followig hatchig. Aalysis of latecy scores also revealed a preferece for the familiar materal call, with chicks showig shorter latecies i their respose to the familiar Call B tha to the ufamiliar Call A (p <.1). These results from the cotrol chicks parallel the results obtaied from commually icubated embryos i a previous study (Lickliter & Hellewell, 92). I that study, chicks that had bee icubated commually ad exposed to Call B as embryos also preferred the familiar materal call over the ufamiliar call variat at 24 hr followig hatchig. The fact that the experimetal chicks i the isolatio-exposure group i the preset experimet did ot lear the idividual materal call as embryos further supports our predictio that the lack of backgroud sesory stimulatio provided by broodmates leads to a isesitivity to the effects of specific preatal experiece. The results of this experimet, combied with those from Experimets 1 ad 2, demostrate the geerality of this isesitivity pheomeo ad suggest the possibility of a geeral arousal-based mechaism. This arousal-based mechaism is presumed to be regulated by some optimal level of overall sesory stimulatio (typically provided by the vestibular, tactile, ad proprioceptive experiece associated with the late stages of icubatio), which makes it possible for the embryo to atted ad respod to additioal sesory experiece preset i the preatal eviromet. Experimet 4: Effects of Cocurret Preatal Isolatio ad Visual Stimulatio o Auditory Learig A recet study usig duck embryos ad hatchligs foud that embryos receivig substatially icreased amouts of preatal vestibular, tactile, ad proprioceptive stimulatio fail to lear a idividual duck materal call (Radell & Gottlieb, 92), Table 3 Preferece of Chicks i Simultaeous Auditory Choice Tests at 24 Hours Followig Hatchig i Experimets 3 ad 4 Group Isolatio-o exposure Isolatio-exposure Commual-exposure (cotrols) Isolatio-cocurret auditory + visual group * p <.1 (chi-square test). 2 2 2 2 respodig 2 Bobwhite Call A (ufamiliar) 8 7 3 Preferece Bobwhite CallB (familiar) 14* 13* No preferece 3 1
INTERSENSORY EXPERIENCE AND PERCEPTUAL DEVELOPMENT 1 whereas duck embryos receivig o augmeted stimulatio or oly slightly augmeted amouts of stimulatio demostrate a postatal preferece for the familiar idividual duck materal call (Gottlieb, Tomliso, & Radell, 89; Radell & Gottlieb, 92). We obtaied a similar failure to lear a idividual materal call i Experimet 3, but i our case this result was obtaied i embryos that received decreased amouts of preatal vestibular, tactile, ad proprioceptive stimulatio as a result of their isolatio from broodmates durig the late stages of icubatio. This fidig suggests that some optimal level of overall sesory stimulatio is required for the developmet of ormal or species-typical perceptual capacity. I other words, it appears that ay substatial deviatio from the rage of sesory stimulatio ormally ecoutered preatally (be it more or less tha ormal) is likely to result i altered patters of perceptual fuctioig. If the rage of stimulatio hypothesis that we have proposed to accout for the results from the previous three experimets is correct, the it should be possible to obtai preatal learig of a idividual materal call by providig icreased sesory stimulatio to physically isolated embryos durig exposure to the call. The purpose of the fial experimet was to examie this possibility by repeatig the procedures of Experimet 3, except that this time i additio to beig exposed to a specific materal call before hatchig, isolated embryos also were exposed to cocurret visual stimulatio. We predicted that if a substatial reductio i the amout of overall sesory stimulatio ormally preset i the preatal eviromet was resposible for the fuctioal deficit see i the prior experimet, the icreasig the amout of sesory stimulatio (regardless of the specific type of stimulatio) available to the embryo durig exposure to the materal call should provide a adequate level or threshold of stimulatio to facilitate preatal auditory learig. Method Twety bobwhite quail embryos, draw from three separate hatches, served as subjects. The experimetal procedures of Experimet 3 were repeated, except that i this experimet subjects also received exposure to a temporally pattered light durig their exposure to the idividual materal call. Specifically, embryos icubated i isolatio were exposed to a 1-W light pulsed at three cycles per secod durig the 1 mi/hr that the materal call was broadcast. Subjects thus received cocurret auditory ad visual stimulatio durig the later stages of icubatio. After hatchig, chicks were placed i social groups cotaiig 1 to 12 same-age chicks ad were idividually tested at 24 hr of age i a simultaeous choice test betwee the familiar bobwhite call (Call B) ad the ufamiliar variat of the call (Call A), as i the Experimet 3. Results ad Discussio As ca be see i Table 3, subjects icubated i isolatio ad exposed to preatal visual stimulatio at the same time they were exposed to a idividual materal call demostrated a sigificat preferece for that familiar call at 24 hr followig hatchig (p <.1). Aalysis of the latecy of respose by the Wilcoxo test also revealed a preferece for the familiar materal call: Subjects showed shorter latecies i their respose to the familiar bobwhite call (Call B) tha to the ufamiliar call (p <.1). This demostratio of idividual auditory learig is i sharp cotrast to the results of Experimet 3, i which embryos icubated i physical isolatio (but ot exposed to visual stimulatio) did ot exhibit a preferece for the familiar materal call ad supports the otio that icreasig the amout of sesory stimulatio available to physically isolated embryos facilitates early auditory learig. The results from the preset experimet likewise differ from the results obtaied from commually icubated bobwhite embryos i a previous study (Lickliter & Hellewell, 92). I that study, commually icubated embryos that received visual stimulatio cocurretly with exposure to the materal call failed to lear that materal call, whereas cotrol embryos that were ot exposed to uusually early visual iput durig exposure to the call did lear the idividual materal call. The fidigs from the preset experimet, which show that exposure to uusually early visual iput i the absece of specific sesory stimulatio from broodmates leads to successful auditory learig, provides yet more evidece that preatal learig requires some optimal level of backgroud stimulatio to be effective. Take together, the results of the preset experimet ad the results of the Lickliter ad Hellewell (92) study idicate that there is some optimal level of overall sesory stimulatio bobwhite embryos require durig the preatal period; substatial icreases (e.g., exposig commmually icubated embryos to cocurret auditory ad visual stimulatio) or substatial decreases (e.g., icubatig embryos i physical isolatio from broodmates) i the rage of stimulatio ormally preset results i deficits i early perceptual fuctioig. A similar coclusio was reached by Radell ad Gottlieb (92) i their study of developmetal itersesory iterferece i ducklig embryos ad hatchligs. As discussed earlier, Radell ad Gottlieb (92) showed that sigificatly augmeted preatal stimulatio of the vestibular, tactile, ad proprioceptive systems ca also iterfere with ormal patters of early auditory learig. Geeral Discussio By way of review, the experimets of this study examied the effects of atteuated preatal sesory stimulatio o subsequet auditory ad visual resposiveess to materal cues i bobwhite quail chicks. Results revealed that chicks deied direct physical cotact with broodmates durig the late stages of icubatio exhibit patters of perceptual fuctioig differet from chicks allowed ogoig vestibular ad tactile stimulatio from broodmates durig late icubatio. Specifically, chicks icubated i physical isolatio respoded to materal auditory cues ito later stages of postatal developmet (Experimet 1) ad failed to respod to materal visual cues at ages ormally reared chicks display such species-specific visual resposiveess (Experimet 2). I additio, embryos icubated i physical isolatio failed to exhibit early auditory learig of a idividual materal call, a behavior reliably see i commually icubated embryos (Experimet 3). However, isolatio-reared embryos receivig visual stimulatio cocurretly with exposure to a idividual materal call did demostrate preatal auditory learig (Experimet 4). These results idicate that a substatial decrease i the amout of sesory stimulatio ormally preset i the preatal
1 ROBERT LICKLITER AND DAVID J. LEWKOWICZ eviromet ca result i altered preatal ad postatal perceptual fuctioig. Specifically, these results demostrate a slowig i the rate of species-specific perceptual developmet whe compared with umaipulated hatchligs. Thisfidigis complemeted by results obtaied i related studies cocered with the effects of substatial icreases i the amout of sesory experiece preset preatally (Gottlieb et al., 89; Lickliter & Hellewell, 92; Radell & Gottlieb, 92). These studies all foud that icreases i the rage of stimulatio ormally preset i the preatal period ca also result i deficits i the early perceptual capacities of avia embryos ad hatchligs. I the more geeral sese, the results of this study are cosistet with a view of perceptual developmet iitially proposed by Scheirla (9, ) over 3 years ago. Scheirla argued that quatitative aspects of sesory stimulatio play a critical role i shapig the behavioral-perceptual repertoire of a orgaism durig its earliest stages of developmet. More pertiet to the preset fidigs, he also maitaied that the effectiveess of a particular stimulus depeds ot oly o its specific quatitative value but also o the properties of the orgaism's receptors, the aimal's geeral state of arousal, its experietial history, ad its developmetal coditio (Scheirla, ). More recetly, a umber of ivestigators have elaborated ad exteded Scheirla's ideas ad have geerated a body of empirical evidece i support of his positio (i.e., Karmel, Garder, & Magao, 91; Lewkowicz, 91; Turkewitz, Lewkowicz, & Garder, 83). The uique role that quatitative aspects of stimulatio play i early sesory-perceptual fuctioig is illustrated by the fidigs of a study by Lewkowicz ad Turkewitz (8). They showed that whe huma ifats are give the opportuity to equate auditory ad visual iputs o the basis of their itesity, they do so without ay prior traiig. The spotaeous propesity to equate stimulatio across modalities o the basis of itesity differs markedly from adults' behavior i the same experimetal task. I cotrast to ifats, adults do ot exhibit spotaeous cross-modal matchig of itesity. Similar evidece of itesity-based, odifferetial respodig to stimulatio from differet modalities by ifats has bee obtaied by Spear ad his colleagues i work with eoatal rat pups (Spear, Kraemer, Molia, & Smoller, 88; Spear & Kucharski, 84; Spear & Molia, 87). Spear ad his colleagues foud that followig the acquisitio of coditioed suppressio to a stimulus i a give modality, rat pups (but ot adults) ca exhibit trasfer of coditioed suppressio to stimuli from other modalities. Such itersesory equivalece appears to be uiquely characteristic of the eoatal period ad is thought to be the result of quatity-based respose mechaisms that mediate behavioral fuctioig durig the earliest stages of developmet (Turkewitz etal., 83). I additio to evidece that itesity of stimulatio provides a basis for itersesory resposiveess durig ifacy, there is also a substatial body of evidece showig that a stimulus of a fixed value ca have markedly differet effects o the eoate depedig o the amout of cocurret stimulatio provided i the same or differet sesory systems or o the eoate's level of arousal. For example, Lewkowicz ad Turkewitz (81) showed that huma ifats' visual prefereces for lights of differet brightess could be modified by first prestimulatig them with a pulse of white oise. Ifats who were prestimulated with soud reduced their lookig at a brighter light ad icreased lookig at the dimmest light compared with a cotrol group of ustimulated ifats. Garder ad Karmel (84) foud that eoates who are tested just after they have bee fed, ad therefore whe their arousal level is relatively low, prefer to look most at rapidly flashig visual stimuli ad look least at slowly flashig oes. I cotrast, the same ifats prefer to look most at slowly flashig visual stimuli whe they are tested i a highly aroused coditio (i.e., just before feedig). Garder, Lewkowicz, Rose, ad Karmel (8) obtaied a similar shift i visual prefereces, but i this case the shift i preferece was obtaied by prestimulatig eoates with either auditory or visual stimulatio before testig for their prefereces. Take together, thesefidigsshow that it is possible to modify the attetioal "value" of a give stimulus or rage of stimuli by maipulatig the ifat's overall level of arousal ad that this modificatio ca be achieved by maipulatig either the orgaism's iteral state or the ature of exteral sesory iputs, regardless of modality. This patter of results has led Karmel et al. (91) to argue that eoatal behavioral resposiveess is the result of a iteractio betwee arousal ad attetioal systems ad that oe system caot be uderstood without cosideratio of the other. I other words, the attetioal value of a give stimulus caot be uderstood simply by referrig to its specific physical attributes. Rather, attetioal value ca oly be uderstood whe it is cosidered withi the overall cotext of the orgaism, icludig the iteractio of both iteral ad exteral sources of stimulatio ad the resultat level of orgaismic arousal. The overall patter of results from the preset experimets is cosistet with this view ad suggests that the perceptual developmet of precocial birds may also be best uderstood by cosiderig the iteractio of attetioal ad arousal systems. As with huma ifats, the respose of bobwhite quail embryos to a specific sesory iput (a idividual materal call) was very differet depedig o whether cocurret sesory stimulatio was preset. Furthermore, the fact that preatal learig of a specific materal call ca be obtaied either i the presece of broodmates (Lickliter & Hellewell, 92) or i the absece of broodmates but i the presece of cocurret visual stimulatio (Experimet 4) idicates the ospecificity of sesory stimulatio levels ecessary for preatal auditory learig to occur. Additioal evidece for this view comes from Radell ad Gottlieb's (92) experimets showig that duck embryos fail to lear a specific duck materal call i the presece of substatially augmeted multimodal stimulatio. These results suggest that whe the sum of stimulatio exceeds some optimal rage, the embryo o loger atteds to the additioal exteral sesory iput provided ad thus does ot icorporate the cosequeces of specific preatal stimulatio ito its subsequet perceptual repertoire. Evidece that demostrates the coverse of this effect comes from Experimets 1 ad 2 of this study. The results from these two experimets show that whe embryos are deprived of the ormally available vestibular, tactile, ad proprioceptive stimulatio provided preatally by broodmates, they do ot atted to augmeted visual stimulatio i a way that allows them to demostrate its cosequeces whe tested postatally.
INTERSENSORY EXPERIENCE AND PERCEPTUAL DEVELOPMENT 17 It is importat to ote that recet results from various ivestigators workig with a variety of aimal ifats (rather tha embryos) have likewise show that sesory overstimulatio or deprivatio ca result i detrimetal effects o the developmet of itersesory itegratio (Forema & Altaha, 91; Key & Turkewitz, 8; McBride & Lickliter, 94; Symos & Tees, 9). However, the data from these studies ad the preset work are ot sufficiet to allow ay a priori predictios regardig the optimal levels or thresholds of stimulatio ecessary for the achievemet of ormal or typical perceptual developmet i embryos or eoates. What remais to be explored i future studies are the specific parameters of arousal-based respose mechaisms that would allow the idetificatio of the levels or thresholds of stimulatio associated with ormal fuctioig ad the uderlyig eural structures resposible for these mechaisms. Refereces Alberts, J. R. (84). 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18 ROBERT LICKLITER AND DAVID J. LEWKOWICZ ferece: Augmeted preatal sesory experiece iterferes with auditory learig i duck embryos. Developmetal Psychology, 28, 79-83. Roca, A. E., Lamki, C. A., & Alberts, J. R. (93). Materal cotributios to sesory experiece i the fetal ad ewbor rat. Joural of Comparative Psychology, 17, 1-14. Scheirla, T. C. (9). A evolutioary ad developmetal theory of biphasic processes uderlyig approach withdrawal. I M. Joes (Ed.), Nebraska symposium o motivatio (Vol. 7, pp. 1-42). Licol: Uiversity of Nebraska Press. Scheirla, T. C. (). Aspects of stimulatio ad orgaizatio i approach/withdrawal processes uderlyig vertebrate behavioral developmet. I D, S. Lehrma, R. Hide, & E. Shaw (Eds.), Advaces i the study of behavior (pp. 1-71). New York: Academic Press. Smotherma, W. P., & Robiso, S. R. (8). Evirometal determiats of behavior i the rat fetus. Aimal Behaviour, 34, 189-1873. Smotherma, W. P., & Robiso, S. R. (87). Psychobiology of fetal experiece i the rat. I N. A. Krasegor, E. M. Blass, M. A. Hofer, & W. P. Smotherma (Eds.), Periatal developmet: A psychobiological perspective (pp. 39-). New York: Academic Press. Spear, N. E., Kraemer, P. J., Molia, J. C, & Smoller, D. (88). Developmetal chage i learig ad memory: Ifatile dispositio for "uitizatio." I J. Delacour & J. C. Levy (Eds.), Systems with learig ad memory abilities (pp. 27-2). Amsterdam: Elsevier/North Hollad. Spear, N. E., & Kucharski, D. (84). Otogeetic differeces i stimulus selectio durig coditioig. I R. Kail & N. E. Spear (Eds.), Comparative perspectives o the developmet.of memory (pp. 227-22). Hillsdale, NJ: Erlbaum. Spear, N. E., & Molia, J. C. (87). The role of sesory modality i the otogey of stimulus selectio. I E. M. Blass, M. A. Hofer, & W. P. Smotherma (Eds.), Periatal developmet: A psychobiological perspective(pp. 83-11). Orlado, FL: Academic Press. Stokes, A. W. (7). Behavior of the bobwhite (Colius virgiiaus). Auk, 84, 1-33. Symos, L. A., & Tees, R. C. (9). A examiatio of the itramodal ad itermodal behavioral cosequeces of log-term vibrissae removal i the rat. Developmetal Psychobiology, 23, 849-87. Turkewitz, G., & Key, P. (82). Limitatios o iput as a basis for eural orgaizatio ad perceptual developmet: A prelimiary theoretical statemet. Developmetal Psychobiology, 1, 37-38. Turkewitz, G., Lewkowicz, D. J., & Garder, J. (83). Determiats of ifat perceptio. I J. Roseblatt, C. Beer, R. Hide, & M. Busel (Eds.), Advaces i the study of behavior (pp. 39-2). New York: Academic Press. Received February 2, 94 Revisio received November, 94 Accepted November, 94