Behavioral response of altricial and precocial rodent fetuses to acute umbilical cord compression

BEHAVIORAL AND NEURAL BIOLOGY 57, 93--102 (1992)

Behavioral Response of Altricial and Precocial Rodent Fetuses to Acute Umbilical Cord Compression SCOTT R . ROBINSON

Department of Zoology, Oregon State University, Corvallis, Oregon 97331 AND

WILLIAM P. SMOTHERMAN 1 Center for Developmental Psychobiology, Department of Psychology, State University of New York at Binghamton, Binghamton, New York 13902-6000

In recent years the view that adaptive behavior is expressed by immature animals at particular times during development, and not just during adulthood, has received increasing attention (A1berts & Cramer, 1988; Oppenheim, 1984). Most studies of ontogenetic adaptation have focused on infants or juveniles, with relatively little attention devoted to developing animals before birth or hatching (cf. Smotherman & Robinson, 1988a; Robinson & Smotherman, 1988). One of the likely reasons that fetal behavioral adaptations have received little attention is that the fetus seems to have all its needs satisfied through a life-support system consisting of the umbilical cord and placenta. Maintenance of this life-support system is crucial to fetal survival and growth. Therefore, one of the most likely places to find behavioral adaptations during the prenatal period is in association with maintenance of a healthy umbilical connection to the placenta. Fetuses are at risk of transient occlusion of blood circulation within the umbilical cord during gestation. Acute fetal hypoxia, induced by umbilical cord compression, has been implicated as an important cause of brain damage in h u m a n fetuses (Mann, 1986) and can occur during unremarkable pregnancies (Itskovitz, LaGamma, & Rudolph, 1987). Accidental cord compression can occur by twisting of the cord as a result of fetal activity or by pinching the cord between the fetus and a hard part of maternal anatomy (such as the pelvis) or, in species that bear multiple offspring, against an adjacent sibling in utero.

Norway rat fetuses (Rattus norvegicus) exhibit a stereotypic behavioral response when the umbilical cord is experimentally compressed with a vascular clamp. In this study, the development of the fetal behavioral response to cord compression was compared in altricial and precocial rodents, which differ markedly in neural and motor maturity at the time of birth. Both altricial and precocial species showed some form of behavioral response to umbilical cord compression. Fetuses of two altricial species, Norway rats and Mongolian gerbils (Meriones unguiculatus), expressed hyperactivity in response to cord compression throughout the last third of gestation. In contrast, precocial cotton rats (Sigmodon hispidus) and spiny mice (Acomys cahirinus) did not respond to cord compression until relatively late in gestation. Thus, altricial and precocial species do not express the cord compression response during comparable periods of neural development: precocial species are much more mature at the earliest expression of this behavior than altricial species. These findings are consistent with the interpretation that the cord compression response is a behavioral adaptation that can promote survival of the fetus in utero. © 1992 Academic Press, Inc.

1 This research was supported in part by G r a n t HD16102 from the National Institute of Child H e a l t h and H u m a n Development (NIH) to W.P.S. and instructional research awards from Oregon State University to S.R.R.W.P.S. is supported by G r a n t HD 00719 from NICHD. All correspondence and reprint requests should be addressed to Scott R. Robinson, Ph.D. a t the Center for Developmental Psychobiology, D e p a r t m e n t of Psychology, P.O. Box 6000, SUNY-Binghamton, Binghamton, NY 139026000. 93

0163-1047/92 $3.00 Copyright © 1992 by Academic Press, Inc. All rights of reproduction in any form reserved.

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ROBINSON AND SMOTHERMAN

Previous investigators have suggested the existence of a behavioral response of fetuses to umbilical cord compression. Many of the early studies of fetal motor development conducted during the 1920s and 1930s were criticized by Windle (1944) as lacking in proper controls to avoid the effects of fetal hypoxia. To support his claim, Windle described a predictable sequence of behavioral changes that occur when fetuses become anoxic. More recently, descriptions of a brief period of fetal hyperactivity following transient hypoxia have been reported in rats (Becker, King, Marsh, & Wyrick, 1964) and dogs (Arshavsky, Ashavskaya, & Praznikov, 1976). Smotherman and Robinson (1987, 1988b) confirmed and extended these previous reports in a series of quantitative experimental investigations of the response of rat fetuses to transient compression of the umbilical cord. They described a three-phase response following placement of a microvascular clamp on the umbilical cord, which completely occludes umbilical circulation. This response consists of (a) initial suppression of fetal activity, (b) an intermediate phase of fetal hyperactivity, in which activity increases four- to fivefold over baseline levels, and (c) a final phase of behavioral suppression in which fetal activity drops to near zero levels until removal of the umbilical cord clamp. The critical feature of this pattern is the second phase--hypera c t i v i t y - w h i c h distinguishes it as an active behavioral response to cord compression. These characteristics of the cord compression response provide a strong prima facie case that it is a behavioral ontogenetic adaptation of the fetus. Although some features of the cord compression response of the rat fetus suggest that it is functional in utero, it is possible that this behavior is merely an incidental consequence of reduced oxygen availability to the nervous and motor systems. For example, a burst of motor activity could result from the disappearance of cortical inhibition of spinal reflexes induced by hypoxia. This "epiphenomenal" hypothesis suggests that the development of the cord compression response should be related to general patterns of neural and behavioral maturation. In the present study, the development of a behavioral response to umbilical cord compression was compared in altricial and precocial species that differ dramatically in neural and motor maturity at the time of birth. Analyses determined the presence or absence of fetal hyperactivity following placement of a vascular clamp on the umbilical cord at different gestational ages in four species of Murid rodents.

METHODS

Subjects Subjects were fetuses produced in timed matings of four species in the rodent family Muridae. Two species, representing the murine and cricetine branches of the family, respectively, give birth to altricial offspring: Norway rats (Rattus norvegicus, the progeny of Sprague-Dawley females bred to Long-Evans males; gestation length = 21 days) and Mongolian gerbils (Meriones unguiculatus; gestation length -- 24 days). The other two species, from the same respective subfamilies, give birth to precocial offspring: spiny mice (Acomys cahirinus; gestation length = 38 days) and cotton rats (Sigmodon hispidus; gestation length = 27 days). The gestational age of fetal subjects was determined by the presence of sperm in a vaginal smear or detection of a copulatory plug in species bred in groups (R. norvegicus and S. hispidus) or by date of birth of the previous litter in species housed as breeding pairs (M. unguiculatus and A. cahirinus). Gestational age was verified by comparison of body mass of all fetuses to standard fetal growth curves for each species. At all times, adult and fetal subjects were maintained and treated in accordance with guidelines established by the National Institutes of Health and the Animal Behavior Society.

Preparation of Fetuses To permit direct observation of fetal behavior, the pregnant female was placed under brief ether anesthesia and a small volume of ethanol (30-100 t~l) was injected into the spinal canal between the first and second lumbar vertebrae, producing complete blockade of the spinal cord in the upper l u m b a r lower thoracic region. The prepared female was placed in a holding device and immersed to chest depth in a buffered physiological saline solution maintained at 37.5°C. This preparation has the effect of eliminating sensation in the lower half of the body of the pregnant female, permitting direct access to fetuses without the use of general maternal anesthesia, which suppresses fetal activity. This general experimental procedure has been employed extensively in previous research on fetal rats (Smotherman, Richards, & Robinson, 1984; Smotherman & Robinson, 1991). The uterus was externalized through a low midline incision in the abdomen. A single fetus was selected as an experimental subject for this study and was externalized into the saline bath through

UMBILICALCORD COMPRESSION a small incision in the uterus. (The data in this report were collected as part of a larger study of fetal development (Robinson, 1989). To minimize the number of pregnant females needed, other fetuses within each pregnancy were used as subjects in different experiments.) Special care was exercised to maintain unimpaired blood circulation within the umbilical cord and intact placental-uterine attachment. All subject fetuses remained pink and welloxygenated until the moment of umbilical cord occlusion. A minimum sample size of five fetuses, each from different pregnancies, was tested in each species at each gestational age. Testing was conducted at the earliest age at which fetuses remained viable after externalization from the uterus: Day 17 for R. norvegicus, Day 19 for M. unguiculatus, Day 26 for A. cahirinus, and Day 18 for S. hispidus. Sample sizes for each gestational age are listed in Table 1. Each subject was tested during a 3-rain observation session. A microvascular clamp, delivering 10-20g compression pressure (Smotherman & Robinson, 1988b) was placed on the proximal end of the umbilical cord 5-10 mm from the fetal abdomen, at the end of the first minute of the session (designated to). The clamp remained in place for 120 s, completely occluding umbilical circulation through the end of the observation session (t12o). Subjects were observed continuously during the session, and each instance of fetal movement was noted and entered into a microcomputer serving as a real-time event recorder, preserving information about the frequency and timing of fetal motor activity. Five categories of fetal movement were distinguished, defined by the region of the fetal body involved in the movement: Forelimb, Rearlimb, Head, Mouth, and Trunk (Smotherman & Robinson, 1986, 1991). The number of fetal movements summed across all five behavioral categories was used as a measure of overall fetal activity.

Activity Analysis The overall motor activity of fetuses during the observation session was divided into a series of 15s intervals for analysis. A baseline activity score (designated "preclamp") was calculated as the mean activity expressed during the minute (four intervals) before placement of the clamp. To measure the /~tal response to umbilical cord compression, activity of fetuses during the period following placement of the clamp was divided into eight 15-s intervals. Fetal activity across these nine scores was analyzed in a one-way repeated measures ANOVA. Where a

95

significant main effect of 15-s intervals was evident (a = .05), a planned comparison using a one-tailed Dunnett t test (Roscoe, 1975) was conducted to determine whether the postclamp interval exhibiting the highest rate of fetal movement was significantly greater than the preclamp baseline. A fetal activity response to umbilical cord compression was judged to be present only if this planned comparison was significant. To further characterize age-related changes in the fetal response to umbilical cord compression, the relative occurrence of different behavioral categories was compared in a series of one-way ANOVAs. The relative occurrence of Forelimb, Rearlimb, Head, Mouth, and Trunk movements was calculated as the frequency of each category observed over the 2-min period following placement of the clamp divided by overall fetal activity during the same period. These analyses incorporated only those ages where a significant increase in fetal activity was noted following placement of the umbilical cord clamp.

Postobservation Measurements At the conclusion of the last observation for a particular litter, the prepared dam was removed from the saline bath, released from the holding device, and quickly euthanized by cervical dislocation. Each conceptus, comprising fetus, placenta, and extraembryonic membranes, was removed promptly from the uterus, whenever possible with intact membranes to permit measurement of amniotic fluid volume. Each fetus was weighed to the nearest 0.01 g before and after removal of amniotic fluid and after removal of placenta, umbilical cord, and extraembryonic membranes to provide separate measurements of the mass of amniotic fluid and the body mass of the fetus. Because the specific gravity of amniotic fluid is nearly equal to water, the mass of amniotic fluid measured in this way was taken as a direct estimate of amniotic fluid volume in milliliters. To measure the combined effects of fetal and amniotic fluid growth or diminution, an index of free space surrounding the fetus was calculated. Free space was defined as the volume of amniotic fluid divided by the sum of the volumes of amniotic fluid and fetal body. RESULTS

Physical Changes in the Intrauterine Environment Body mass exhibited continuous increase with gestational age in all four species. In R. norvegicus,

96

ROBINSON

AND SMOTHERMAN

BodyMass R. norvegicus

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Gestational Age (days)

FIG. 1. Changes in fetal body mass (left axis) and amniotic fluid volume (right axis) from the inception of fetal movement through term in four Murid rodents. The four graphs are grouped to reflect differences in development (altricial, top row; precocial, bottom row) and taxonomic lineage (murine, right column; cricetine, left coloumn). Points represent means; vertical bars show SEM. fetal mass increased ninefold (9.0 x ) from the inception of fetal movement on Day 16 through term on Day 21 (Fig. 1). This compares with increases of 7.9, 13.5 and 11.1 x in M. unguiculatus, A. cahirinus, and S. hispidus, respectively. Amniotic fluid appeared to increase and then decrease in volume in R. norvegicus (Fig. 1). A significant effect of gestational age was evident (F(5, 22) = 25.1, p < .001). Post hoc comparisons revealed a significant increase in amniotic fluid volume from Days 16 through 18. Fluid volume remained near this peak for a day, then declined dramatically through term. The volume of fluid on Day 21 was only 26% of the peak achieved on Day 18. Significant variation in amniotic fluid volume during the last third of gestation also was evident in M. unguiculatus (F(6, 23) = 7.0, p < .001). However, post hoc examination indicated that this variation was entirely attributable to a sudden decrease in fluid volume on the last day of gestation. No significant fluctuation in fluid volume occurred over the period of Days 18-23. Amniotic fluid was sampled at five ages in A. cahirinus: Days 22, 26, 30, 34, and 37. Over this period, fluid appeared to vary in volume (F(4, 10) = 3.8, p < .05). Post hoc tests found a significant difference only between the peak of fluid volume on Day 30 and its nadir (32% of peak volume) on Day 37. In S. hispidus, amniotic fluid was already near its peak volume at the beginning of the fetal period (Day 17). The significant change in fluid volume (F(10, 45) = 10.8, p < .001) was found to be due to a steady decrease after Day 23. At term (Day 27), amniotic fluid volume was only 16% of the peak on Day 18.

The index of free space varied significantly with gestational age in R. norvegicus (F(5, 22) = 176.0, p < .001). F r e e space diminished monotonically over the period from a m a x i m u m of 31% on Day 16 to a minimum of 3% on Day 21. The rate of decline was greatest from Day 19 through term. Free space also decreased steadily from Day 18 through term in M. unguiculatus (F(6, 23) = 59.7, p < .001). This trend occurred in spite of the relative stability of amniotic fluid volume, indicating that the major component of the index is increasing fetal mass, accentuated by disappearing amniotic fluid near term. Free space declined from a m a x i m u m of 26% to a minimum of 3% at term. The same trend of diminishing free space was evident among the five calculable ages in A. cahirinus (F(4, 10) = 32.5, p < .001). Free space was greatest (32%) on Day 22 and least (3%) on Day 37. In S. hispidus, free space exhibited a significant decline from 46% on Day 17 to 2% on Days 26 and 27 (F(10, 45) = 73.0, p < .001). The sharpest relative decrease occurred between Days 23 and 24.

Effects of Cord Compression on Fetal Activity Statistical analyses revealed a strong behavioral response to experimental umbilical cord compression at all five ages tested in R. norvegicus (Table 1). The three-phase pattern of behavioral suppression, activation, and suppression was clearly evident (Fig. 2). In M. unguiculatus, fetal hyperactivity following placement of the clamp also was evident at all ages tested. The overall pattern of activity change appeared virtually identical to that exhib-

97

UMBILICAL CORD COMPRESSION

TABLE 1 Fetal Motor Activity (movements/15-s, means _+ SEM) during Baseline and at the Peak of Activity after Umbilical Cord Compression R. norvegicus Day N Baseline Peak Response?

17 5 3.7-+1.3 10.2-+2.3 **

18 5 3.6-+1.5 14.8-+4.1 **

19 5 3.5-+0.7 23.8-+2.8 **

20 5 3.9-+0.6 21.2-+2.9 **

21 5 3.6-+1.2 12.8-+4.8 *

19 5 4.8-+0.9 13.0-+2.3 **

20 5 4.2-+1.0 10.6-+2.7 *

21 5 3.0-+1.0 10.4-+2.9 **

22 5 4.0-+1.1 12.8-+2.4 **

23 24 5 6 3.5+_0.6 4.3-+1.0 1:.4-+ 1.8 11.2-+1.9 ** **

26 5 1.4-+0.5 2.4-+1.1 NS

28 5 1.4-+0.6 3.4-+1.3 NS

30 5 3.3-+1.3 2.6-+0.6 NS

32 5 1.7+0.4 4.4-+0.7 *

34 5 1.5-+0.8 6.0_+1.9 *

37 5 0.3-+0.1 3.0-+0.9 *

18 5 0.7-+0.3 0.8-+0.6 NS

19 5 1.0-+0.3 1.4-+0.8 NS

20 6 3.2-+1.2 2.8-+1.3 NS

21 11 2.6-+1.0 3.3-+1.1 NS

22 5 4.5_+2.0 6.4_+1.7 NS

23 24 5 5 2.8_+1.3 5.3-+1.9 6.2_+1.9 16.4-+1.6 *

M. unguiculatus Day N Baseline Peak Response?

A. cahirinus Day N Baseline Peak Response?

S. hispidus Day N Baseline Peak Response?

25 5 4.3-+1.5 12.6-+2.7

26 27 6 5 2.7_+0.9 0.8-+0.4 16.8+_2.9 15.6-+2.9

Note. Results of planned comparisons of fetal response employing the Dunnett t statistic are presented as NS (not significant), *(p < .05), or **(p < .01).

i t e d b y R . norvegicus, w i t h l o w r a t e s of m o v e m e n t occurring both before a n d after the h y p e r a c t i v e phase. T h e r e s u l t s of u m b i l i c a l c l a m p t e s t s i n d i c a t e d t h a t A. cahirinus fetuses exhibited a behavioral response

27 24

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to u m b i l i c a l cord c o m p r e s s i o n o n l y a t l a t e r g e s t a t i o n a l a g e s . N o s i g n i f i c a n t r e s p o n s e to u m b i l i c a l cord c o m p r e s s i o n w a s f o u n d f r o m D a y s 26 t h r o u g h 30, b u t s i g n i f i c a n t m a i n effects a n d p l a n n e d comp a r i s o n s w e r e n o t e d o n d a y s 32, 34, a n d 37. H o w -

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15

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60

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105 120

Time (s) FIG. 2. Temporal changes in overall fetal activity during the 120-s period after cord compression. A typical graph, depicting the fetal response at a single age, is presented for each of the four Murid species. Points represent the mean number of fetal movements per 15-s interval; vertical bars depict SEM.

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Gestational Age (days) FIG. 3. Relative abundance of five categories of fetal movement, expressed as a percentage of overall fetal activity, after cord compression in four Murid species. ever, the number of behavioral acts exhibited during the peak of the hyperactive phase appeared substantially smaller than that seen in the other three species. S. hispidus fetuses exhibited a behavioral response to umbilical cord compression that included a phase of hyperactivity, b u t this response was not evident at all ages. No response at all was evident from Days 18 through 22. At all subsequent ages, a significant increase in fetal activity was observed following placement of the umbilical cord clamp.

Motor Patterns Associated with Cord Compression Response No significant variation was apparent in the relative occurrence of forelimb, rearlimb, head, or trunk movements over Days 17-21 in R. norvegicus. A significant result for mouth activity (F(4, 20) = 3.3, p < .05) indicated that mouth movements occurred relatively more frequently on Day 21 than on Day 17. At no age, however, did mouth movements constitute more than 10% of overall activity. The modal category of behavior at all ages was t r u n k activity, which overwhelmingly consisted of vigorous lateral curling or bending movements. Trunk curls were the most abundant form of movement at all ages (Fig. 3). Forelimb and head movements also were relatively common. Most head movements involved rapid dorsiflexion of the neck, which resulted in a rostral extension of the head ("head toss"). Several instances were noted in which forelimbs were extended together in a rostral direction. Head tosses and rostral forelimb extension were rarely seen during spontaneous fetal activity.

In M. unguiculatus, none of the five categories of movement varied as a function of age. The modal category of response involved head movements, which was the most abundant form of movement at all ages. Many of these head movements involved rostral extension similar to that observed in R. norvegicus. Forelimb movements also occurred commonly, although the paired rostral extension of forelimbs was not observed. Rearlimb, mouth, and, curiously, t r u n k curl movements were relatively uncommon. In fact, t r u n k curls overall accounted for less than 2% of fetal activity that occurred in response to umbilical cord compression. Analyses of components revealed a significant effect of age on rearlimb activity in A. cahirinus (F(2, 12) = 4.4, p < .05). Rearlimb movements were relatively more common on Day 37 than on Day 32. Particularly in older fetuses (Days 34-37), rearlimb movements appeared well-organized, involving vigorous extension of both legs or alternated kicking of each leg in a caudal direction. A significant finding was also obtained for mouth activity (F(2, 12) = 36.2, p < .001), which decreased in relative occurrence from Days 32 through 37. Mouth movements were the most abundant category of movement on Day 32 and rearlimb the most abundant on Days 34 and 37. Other categories of movement, including forelimb, head, and trunk, occurred less often and showed no significant variation with age. Forelimb movements, although not numerous, were particularly notable, as they often involved a slow withdrawal of the forelegs to the chest, bringing the paws close to the head and neck, followed by a gradual extension of both forelimbs in a rostral direction

99

UMBILICAL CORD COMPRESSION

along either side of the head. This deliberate movement, which resembled the forelimb extension pattern evident in R. norvegicus, appeared highly coordinated, the fetus often remaining in the extended posture for several seconds. Other organized patterns of movement, such as head tosses and lateral t r u n k curls, were not evident. S. hispidus fetuses exhibited relatively more t r u n k curls on Day 23 t h a n at other ages (F(4, 21) = 5.0, p < .01). A significant difference was found for the relative occurrence of rearlimb movements (F(4, 21) = 3.3, p = .032), which indicated t h a t rearlimb activity was less common Day 23 t h a n at later ages. No significant variation with age was evident for forelimb, head, or mouth activity. Overall, the most a b u n d a n t category of behavior was rearlimb. Typically, rearlimb movements took the form of a vigorous, synchronous caudal extension of both legs. Often it was noted t h a t the two feet were placed on opposite sides of the umbilical cord during the kicking movement, although it was not apparent whether this foot placement was coincidental or coordinated. Trunk movements were the most abundant category of movement on Day 23 and the second most common movement at subsequent ages. Trunk movements consisted predominantly of lateral body curls, which appeared very similar to those observed in R. norvegicus. Forelimb and head movements occurred relatively less often and mouth activity was virtually absent.

0.5 * [] ----o---

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R. norvegicus M. unguiculatus A. c,ahi.rinus

0.3 09 0.2

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Relative Gestational Age

Comparison across Species

FIG. 4. Changes in an index of intrauterine free space (upper) and the peak of fetal activity followingcord compression (bottom) in four Murid species. Free space is calculated as the volume of amniotic fluid divided by the sum of the volumes of the fetus and fluid. Peak fetal activity was definedfor each gestational age as the maximum rate of fetal movement per 15-s interval after umbilical cord compression. To facilitate species comparison, gestational age is expressed as a fraction of the fetal period for each species, with the inceptionof movementequal to 0.0 and term equal to 1.0. Note that the cord compression response is expressed earlier than the sharp decline in free space, especially in altricial species.

Comparing age-dependent changes across species is a general problem in the comparative study of 8Towth processes, solutions for which have been approached in various qualitative (e.g., Gould, 1977) or quantitative (e.g., Eisenberg, 1981) ways. Most commonly, corresponding points during development have been set as equal, such as the time of conception or the time of birth. Because the focus in the present study is development during the fetal period, ranging from the earliest age at which movement is expressed through term, actual gestational age for each species was converted to a fraction of the fetal period, referred to as relative fetal age, ranging from the inception of movement (0.0) to term (1.0). Changes in a dependent variable were then plotted against this common age scale. However, this method of depicting developmental changes in species with gestation periods of different length did not permit formal statistical comparison across species. As defined above, the free space available to a

fetus in utero is determined by the volume of amniotic fluid and the body mass of the fetus. Changes in free space in all four species as a function of relative fetal age are depicted in Fig. 4. Although S. hispidus began the fetal period with a higher ratio of amniotic fluid to total conceptus volume, free space was essentially equal across species during the last two-thirds of the fetal period. When plotted on the same relative age scale, fetuses of different species did not exhibit the same developmental pattern of the behavioral response to umbilical cord compression. To facilitate comparison, fetal responsiveness to cord compression was expressed as the peak of fetal activity at each gestational age. Peak fetal activity was defined as the 15- s interval after placement of the clamp t h a t comprised the m a x i m u m rate of fetal movement (e.g., 60 s after the clamp in R. norvegicus on Day 19, see Fig. 2). Unlike changes in free space in utero, peak fetal activity after umbilical cord compression

100

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exhibited different ontogenetic trajectories in the four rodent species (Fig. 4). Specifically, a behavioral response to cord compression was evident relatively earlier in the two altricial species, being expressed in both R. norvegicus and M. unguiculatus at the earliest age tested. In contrast, a significant activity response did not appear in the two precocial species until midway through the fetal period, on Day 32 in A. cahirinus (0.67 relative gestational age) and Day 23 in S. hispidus (0.60 relative gestational age). In all four species, however, a significant increase in behavioral activity in response to umbilical cord compression was evident earlier in gestation than the precipitous decline in amniotic fluid volume and free space in utero. DISCUSSION On the basis of experiments conducted with Norway rat fetuses over Gestational Days 19-21, Smotherman and Robinson (1988b) concluded that the umbilical clamp response is a likely candidate for an ontogenetic adaptation that occurs during the prenatal period. The vigorous lateral trunk curls and rostral head extensions described for rat fetuses in previous reports, and replicated in the present study, could well serve to alleviate the cause of accidental cord compression in utero by exerting force against adjacent siblings or hard portions of maternal anatomy. Indeed, vigorous activity during episodes of hypoxia would be maladaptive if it did not help to reverse cord compression because it would more quickly deplete limited oxygen reserves. Fetal hyperactivity also contrasts with the response of neonatal rats to acute hypoxia, which involves an increase in the rate of ventilation and suppression of other motor activity (Eden & Hanson, 1987). The present study identified a behavioral response to umbilical cord compression by fetuses of all four rodent species. The activity response was very similar among R. norvegicus, M. unguiculatus, and older S. hispidus fetuses. In contrast, A. cahirinus fetuses exhibited only a modest increase in overall activity at later ages (Days 32-37). This reduction of hyperactivity, which characterizes the second phase of the clamp response in three species, suggests that the umbilical cord response is less well developed in A. cahirinus or is more similar to the hypoxia response exhibited by infant rodents after birth (Eden & Hanson, 1987). Increased motor activity was a consistent feature of the fetal response to umbilical cord compression across species. However, the phase of hyperactivity

comprised different combinations of motor components in each of the four species. Four organized motor patterns that are rarely or never seen during nonevoked activity or chemosensory stimulation (Smotherman & Robinson, 1986; Robinson, 1989) were identified following umbilical cord compression: rapid bouts of lateral trunk curls, head tosses, synchronous rostral forelimb extensions, and synchronous caudal rearlimb extensions. None of these patterns was unique to one species, but none was seen in all four species. Some patterns appeared to correlate with altricial-precocial differences: head tossing was observed only in altricial species (R. norvegicus and M. unguiculatus), while synchronous caudal extension of the rearlimbs was observed only in precocial species (A. cahirinus and S. hispidus). Other motor patterns appeared to be influenced by taxonomic relationship (rostral extension of the forelimbs occurred occasionally in R. norvegicus and commonly in A. cahirinus). The most vigorous behavioral pattern lateral trunk curls--was observed only in R. norvegicus and S. hispidus, which may indicate that factors other than neural maturity and taxonomy influence the form of the motor response. Although responses varied in form, all patterns of motor activity evoked by cord compression shared two characteristics: they appeared to be very vigorous, in contrast to most other fetal movements, and they involved motion that was directed outward, away from the main axis of the body. The expression of vigorous outward-directed responses to cord compression by all four species is consistent with the idea that this behavior is adaptive during the prenatal period. Precocial species are much more mature at birth than altricial species; both A. cahirinus and S. hispidus are furred, open their eyes, and exhibit adultlike locomotor and grooming behavior during the first 24 h after birth. Precocial fetuses exhibit prenatal patterns of brain development that altricial species do not exhibit until after birth (Brunjes, 1989). Accelerated patterns of brain development, measured relative to the time of birth, are correlated with the early expression of behavior in precocial species. Precocial fetuses at term exhibit neural and motor capabilities that altricial species do not express until 1-2 weeks after birth. Similarly, responsiveness to sensory stimulation is expressed 12 weeks before birth in both A. cahirinus and S. hispidus, but comparable behavioral responses are not evident in R. norvegicus and M. unguiculatus until near term (Robinson & Smotherman, in press). These findings imply parallel patterns of neural and

UMBILICAL CORD COMPRESSION b e h a v i o r a l m a t u r a t i o n in altricial a n d precocial species t h a t differ only in t h e t i m i n g of b i r t h (cf. Brunjes, 1990). One m i g h t expect t h a t t h e ability of fetuses to express a b e h a v i o r a l response to umbilical cord compression would be s i m i l a r l y r e l a t e d to g e n e r a l p a t t e r n s of n e u r a l a n d b e h a v i o r a l m a t u r a t i o n . T h e response to cord compression could, for example, r e s u l t from the release of spinal reflexes as a consequence of r e d u c e d o x y g e n supply to t h e brain. If t h e cord compression response w e r e m e r e l y the c h a n c e consequence of m a t u r a t i o n , it should be expressed in g e s t a t i o n r e l a t i v e l y e a r l i e r in precocial t h a n in altricial fetuses. H o w e v e r , t h e r e s u l t s of this s t u d y indicated t h a t t h e opposite d e v e l o p m e n t a l p a t t e r n occurs. R . norvegicus a n d M. u n g u i c u l a t u s b o t h expressed a significant c h a n g e in a c t i v i t y in response to cord compression a t all g e s t a t i o n a l ages tested, b e g i n n i n g only 1 d a y a f t e r t h e inception of m o v e m e n t (0.17 a n d 0.20 r e l a t i v e g e s t a t i o n a l ages respectively). In contrast, S. h i s p i d u s a n d A . cahirinus failed to e x h i b i t a response d u r i n g t h e first h a l f of t h e fetal period and e x p r e s s e d a n increase in act i v i t y only over t h e last 5 - 6 days of g e s t a t i o n (at 0.60 a n d 0.67 r e l a t i v e g e s t a t i o n a l ages, respectively). T h e cord compression response was not expressed in t h e s e precocial species at e a r l i e r ages w h e n o t h e r p a t t e r n s of coordinated m o t o r b e h a v i o r c o m m o n l y occur (Robinson, 1989). Some form of b e h a v i o r a l response to umbilical cord compression was e x p r e s s e d by all four species observed in this study. T h e form a n d vigorous expression of t h e s e responses d i f f e r e n t i a t e d this response from typical p a t t e r n s of n o n e v o k e d a c t i v i t y in r o d e n t fetuses ( S m o t h e r m a n & Robinson, 1986). Because this b e h a v i o r a l response was e x p r e s s e d soon a f t e r the inception of m o v e m e n t in altricial fetuses, b u t was d e l a y e d u n t i l m o r e a d v a n c e d gest a t i o n a l ages in precocial species, it does not a p p e a r to be associated w i t h g e n e r a l p a t t e r n s of n e u r a l a n d b e h a v i o r a l m a t u r a t i o n . All of t h e s e findings are consistent w i t h a n i n t e r p r e t a t i o n t h a t t h e form a n d d e v e l o p m e n t a l t i m i n g of the cord compression response h a v e b e e n shaped by e v o l u t i o n a r y processes (Gould, 1977). T h e fetal response to umbilical cord compression a p p e a r s to be a f u n c t i o n a l ontogenetic a d a p t a t i o n t h a t p r o m o t e s the s u r v i v a l of t h e fetus in u t e r o (Oppenheim, 1984; S m o t h e r m a n & Robinson, 1988b). REFERENCES Alberts, J. R., & Cramer, C. P. (1988). Ecology and experience: Sources of means and meaning of developmental change. In

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E. M. Blass (Ed.), Handbook of behavioral neurobiology, vol. 9, Developmental psychobiology and behavioral ecology (pp. 1-39). New York: Plenum Press. Arshavsky, I. A., Arshavskaya, E. I., & Praznikov, V. P. (1976). Motor reactions during the antenatal period correlated with the periodic change in the activity of the cardiovascular system. Developmental Psychobiology, 9, 343-352. Becker, R. F., King, J. E., Marsh, R. H., & Wyrick, A. D. (1964). Intrauterine respiration in the rat fetus. 1. Direct observations--Comparison with the guinea pig. American Journal of Obstetrics and Gynecology, 90, 236-246. Brunjes, P. C. (1989). A comparative study of prenatal development in the olfactory bulb, neocortex and hippocampal region of the precocial mouse Acomys cahirinus and the rat. Developmental Brain Research, 49, 7-25. Brunjes, P. C. (1990). The precocial mouse, Acomys cahirinus. Psychobiology, 18, 339-350. Eden, G. J., & Hanson, M. A. (1987). Maturation of the respiratory response to acute hypoxia in the newborn rat. Journal of Physiology, 392, 1-9. Eisenberg, J. F. (1981). The mammalian radiations: An analysis of trends in evolution, adaptation, and behavior. Chicago: University of Chicago Press. Gould, S. J. (1977). Ontogeny and phylogeny. Cambridge, MA: Belknap Press. Itskovitz, J., LaGamma, E. F., & Rudolph, A. M. (1987). Effects of cord compression on fetal blood flow distribution and 02 delivery. American Journal of Physiology, 252, H100-H109. Mann, L. I. (1986). Pregnancy events and brain damage. American Journal of Obstetrics and Gynecology, 155, 6-9. Oppenheim, R. W. (1984). Ontogenetic adaptations in neural development: Toward a more 'ecological' developmental psychobiology. In H. F. R. Prechtl (Ed.), Continuity of neural functions from prenatal to postnatal life (pp. 16-30). New York: Lippincott. Robinson, S. R. (1989). A comparative study of prenatal behavioral ontogeny in altricial and precocial Murid rodents. Unpublished doctoral dissertation, Oregon State University. Robinson, S. R., & Smotherman, W. P. (1988). Chance and chunks in the ontogeny of fetal behavior. In W. P. Smotherman & S. R. Robinson (Eds.), Behavior of the fetus, (pp. 95-115). Caldwell, NJ: Telford Press. Robinson, S. R., & Smotherman, W. P. (in press). Motor competition in the prenatal ontogeny of species-typical behaviour. Animal Behaviour. Roscoe, J. T. (1975). Fundamental research statistics for the behavioral sciences, 2nd ed. New York: Holt, Rinehart and Winston. Smotherman, W. P., Richards, L. S., & Robinson, S. R. (1984). Techniques for observing fetal behavior in utero: A comparison of chemomyelotomy and spinal transection. Developmental Psychobiology, 17, 661-674. Smotherman, W. P., & Robinson, S. R. (1986). Environmental determinants of behaviour in the rat fetus. Animal Behaviour, 34, 1859-1873. Smotherman, W. P., & Robinson, S. R. (1987). Stereotypic behavioral response of rat fetuses to acute hypoxia is altered by maternal alcohol consumption. American Journal of Obstetrics and Gynecology, 157, 982-986. Smotherman, W. P., & Robinson, S. R. (1988a). The uterus as

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Smotherman, W. P., & Robinson, S. R. (1991). Accessibility of the rat fetus for psychobiological investigation. In H. N. Shair, G. A. Barr, & M. A. Hofer (Eds.), Developmental Psychobiology: New Methods and Changing Concepts (pp. 148164). New York: Oxford Univ. Press. Windle, W. F. (1944). Genesis of somatic motor function in mammalian embryos: A synthesizing article. Physiological Zoology, 17, 247-261.