Fetal Antecedents of Infant Temperament
Janet A. DiPietro, Deniee M. Hodgson,
and Kathleen A. Costigan
Johns Hopkins University
Timothy R. B. Johnson
University of Michigan
DiPiETBO, JANET A.; HODGSON, DENICE M.; COSTIGAN, KATHLEEN A.; and JOHNSON, TIMOTHY R. B.
Fetal Antecedents of Infant Temperament. CHILD DEVELOPMENT, 1996,67,2568—2583. This study
established the emergence of stable individual differences in neurobehavioral functioning prior
to birth and examined their relation to subsequent infant temperament. Fetal heart rate and
movement were recorded longitudinally for 31 fetuses at 6 gestational ages beginning at 20
weeks' gestation. Maternally reported temperament data were collected at 3 and 6 months.
Moderate stability in all measures except reactivity was apparent at some time before birth. By
36 weeks, fetal neurobehavior accounted for between 22% and 60% of the variance in prediction
of temperament scores. In general, more active fetuses were more difficult, unpredictable, unadaptable, and active infants. Higher fetal heart rate was associated with lower emotional tone,
activity level, and predictability. We conclude that features of fetal neurobehavior provide the
basis for individual differences in reactivity and regulation in infancy.
How early in the fetal period are differences
between individuals detectable, and to what extent are such differences prognostic of differences
in childhood, or even at maturity? (Sontag & Richards, 1938, p. 65)
The question posed at the conclusion
of the report on the Fels Study of fetal activity remains unanswered but at the core of
current theories of infancy, in which temperament and other psychobiologic aspects of
functioning are implicitly or explicitly
viewed as constitutional in nature. Individual differences in autonomic, motor, state,
and interactive functioning exist in full-term
and preterm neonates shortly after birth, and
adaptation to the extrauterine environment
is predicated on the transaction between
these constitutional characteristics and the
features of the environment subsequently
encountered (Brazelton, 1990; Korner et al.,
1989; Thelen, 1990).
Efforts to validate the construct of individual differences have been directed at
showing stability over time (Rothbart, 1986),
identifying physiologic substrates of behavioral or temperamental variation (Fox, 1989),
and predicting later performance from early
characteristics (Lee & Bates, 1985). Although the bebavioral repertoire of the fetus
near term is similar to that of the newborn
(Prechtl, 1984), limited access to the fetus
has prohibited extensive investigation of the
origins of individual variation in psychobiologic and temperamental function. Demonstration of stable individual differences that
predict or are continuous with postnatal
function would serve to validate many current ontogenic assumptions. A few studies
have investigated the continuity between
specific aspects of fetal and infant functioning, with mixed results. Significant correlations between fetal and infant heart rate
through the first year of life, and heart rate
variability tbrough the first month have been
documented (Lewis, Wilson, Ban, &
Baumel, 1970), and a retrospective study of
11,000 children found a small, but significant, relation between fetal and cbildhood
heart rate at age 10 (Thomas, Haslum, MacGillivray, & Golding, 1989). No significant
relations have been demonstrated between
maternally perceived fetal movements and
infant motor activity measured through observation (Shadmi, Homburg, & Insler,
1986) or mechanical aetometers (Eaton &
This research was supported by grant R29 HD27592, National Institute of Ghild Health
and Human Development, awarded to the first author. The investigators wish to thank the diligent and generous participation of our study families, without which this research would not
have been possible. Address reprint requests to: Janet DiPietro, Department of Maternal and
Ghild Health, Johns Hopkins University, 624 N. Broadway, Baltimore, MD 21205.
[Child Development, 1996,67,2568-2583. © 1996 by the Society for Research in Child Development, Inc.
AH rights reserved. 0009-3920/96/6705-0042$01.00]
DiPietro et al.
McKeen, 1987). Similarities between fetal
and neonatal spontaneously generated cyclic motility (Robertson, 1987) and responsivity to auditory stimuli (Kisilevsky & Muir,
1991) have been documented, but these
studies do not provide data on intraindividual consistency.
Limited success has been achieved in
predicting postnatal functioning from antenatal measures. Better fetal habituation has
been associated witb higher Mental Development Index at 4 months (Madison, Madison, & Adubato, 1986). Intrapartum patterns
of fetal heart rate response to labor have
been associated witb some aspects of neonatal behavioral organization (Emory & Noonan, 1984) and developmental outcome
through age 1, but not later (Painter, Scott,
Hirsch, O'Donoghue, & Depp, 1988). However, these are single study findings, and the
results have not been replicated.
We bave reported data on the ontogeny
of heart rate and variability, motor activity,
behavioral state, and reactivity to stimuli in
the fetus from 20 weeks through term using
Doppler-based actocardiotocography (DiPietro, Hodgson, Costigan, Hilton, & Johnson, 1996, in this issue). These fetal measures are empirically and conceptually
consistent with existing constructs of early
infant individual differences and later infant
temperament. All are parcel of many temperament taxonomies (see Hubert, Wachs, Peters-Martin, & Gandour, 1982, and Rothbart
& Mauro, 1990, for reviews), which have
demonstrated at least moderate levels of
postnatal stability (Colombo, Moss, & Horowitz, 1989; Rothbart, 1986; Stifter & Fox,
1990; Worobey & Blajda, 1989), and there
are reasons to suspect a biologic basis for
each (Fox, 1989; Kagan, Reznick, & Snidman, 1987; Korner et al, 1989; Saudino &
Eaton, 1991). Although there are other temperamental characteristics which fulfill
these criteri.a, fetal reseeirch is limited to
only those features of neurobehavior which
can be reliably measured in the fetus.
In addition, two measures of fetal cardiac function are of interest: heart rate and
hesirt rate variability. Both have been used
extensively in investigations of psychophysiologic processes which may mediate infant
behavior and temperament and are moderately stable during infancy (DiPietro,
Caughy, Cusson, & Fox, 1994; Izard et al.,
1991). Greater variability in heart rate and/
or higher vagal tone have been associated
witb greater emotional reactivity, irritability.
2569
and difficultness in infancy (DeGangi, DiPietro, Greenspan, & Porges, 1991; Fox,
1989; Porges, Doussard-Roosevelt, & Maiti,
1994; Stifler & Fox, 1990). Faster and less
variable heart rate has also been associated
with greater behavioral inhibition (specifically, shyness from the second through fifth
years of childhood; Kagan et al., 1987), although this relation has not been consistendy documented (Kagan, Reznick, & Gibbons, 1989). Preliminary evidence suggests
a relation between higher antenatal heart
rate and a tendency to react with high motoric activity and crying to a series of novel
stimuli at 4 months, a pattern of behavior
characterized by a low tbreshold to novelty
which may ultimately be associated with an
inhibited temperamental style (Snidman,
Kagan, Riordan, & Sbannon, 1995).
Two main hypotheses were generated
for this investigation. First, stability within
each of these measures will emerge prior to
birth, and second, insofar as fetal functioning represents individual differences in neural activation and regulation, these measures
will predict infant temperament. We expected that the strongest relations would be
found between measures that index the
same construct at both times (i.e., greater fetal activity will be associated with greater
infant activity; poorer fetal state regulation,
characterized by fewer periods of state parameter concordance and greater state lability, will predict poorer state control in infancy).
Method
Fetal Data Collection
Details of the study sample and fetal
data collection methods are presented in DiPietro et al. (1996, in this issue). Briefly, subjects were 31 healthy, volunteer pregnant
women and their fetuses. Eligibility was restricted to nonsmoking, bigh school graduates with unremarkable pregnancy histories.
The final sample was composed of welleducated, employed women (M maternal
age = 28.4 years, SD = 3.7; M years education = 16.6, SD — 2.0), with good pregnancy
dating information, and the majority were
primiparous (61%). All newborns were delivered at term, considered healthy, and discharged on normal nursery schedules. Seventeen (55%) were girls.
Subjects were monitored at 20, 24, 28,
32, 36, and 38^39 weeks' gestation using a
single Doppler transducer, applied to the
maternal abdomen, for 50 min. After at least
2570
Child Development
15 min of undisturbed recording, a control
and actual application of a mild vibratory
stimulus (VS) followed (Toitu Fetal Stimulator, TR-30) in random order. Following a 2min period of low fetal beart rate (FHR) variability (approximately 5—10 bpm), the fetal
stimulator was placed on the maternal abdomen near the fetal head and either activated
for 3 sec (i.e., VS) or not activated (i.e., control). Each episode was spaced at least 2 min
apart, and the second event (either stimulus
or control) did not commence until the FHR
returned to baseline. Fetal monitoring continued undisturbed for the remainder of the
50 min. Women were allowed to view the
polygraphic output of the monitor and were
provided with reassurance concerning fetal
well-being but were not given specific feedback on variables which were under investigation as predictors of temperament.
Fetal heart rate and movement data
were collected from a fetal actocardiograph
(Toitu MT320, Wayne, PA). Reliability of
this monitor to accurately detect fetal movement has been established (Besinger &
Johnson, 1989; Maeda, Tatsumura, & Nakajima, 1991). Data were digitized and collected on-line. Fetal heart rate data were
processed through an artifact rejection program and then quantified as (a) mean fetal
heart rate and (b) mean short-term fetal heart
rate variability (i.e., the standeird deviation
of FHR for each 1-min epoch averaged over
the 50-min recording). Fetal heart rate and
FHR variability reactivity were computed as
the change in these measures from the 30
sec preceding to the 30 sec following the VS
and control events. In addition, the duration
of the cardiac response (i.e., once FHR exceeded 5 bpm above baseline, the length of
time it took to return to within 5 bpm of FHR
baseline for at least 5 sec) was calculated.
These two measures were multiplied to
yield a single measure of the magnitude of
the response to the stimulus. Fetal movement (FM) bouts were defined as commencing eacb time the actograph signal attained
or exceeded a predetermined value and terminating when the signal fell below this
level for at least 10 consecutive seconds.
The number of movement bouts was quantified and multiplied by tbeir mean duration,
resulting in a measure of fetal activity (total
amount of minutes the fetus was moving
during the recording). The FM data were not
used in examining the effect of the VS because a low or stable level of FM was not a
criterion for application of the VS.
In addition to digitized data, the polygraphic output of the monitor was used to
score FHR and FM patterns. The FHR patterns were coded in 3-min windows in accord with protocols developed by other investigators to define fetal behavioral states
(van Vliet, Martin, Nijhuis, & Prechtl, 1985),
using existing criteria for patterns A, B, C,
and D. The FM scoring, also in 3-min epochs, was developed by us to be compatible
with the movement categories which are associated with fetal state. Four categories (1
= none or minimal isolated activity; 2 =
mostly inactive, with sporadic gross movements; 3 = frequent activity of moderate
amplitude; and 4 = continuous, high amplitude movement) were distinguished. Intercoder reliability was established. A second FM variable, fetal activity periodicity,
was quantified based on this procedure. This
was the number of times a fetus changed
from a quiescent activity pattern (i.e., FM
pattern 1 or 2) to an active one (i.e., FM pattern 3 or 4). Finally, specific FHR-FM patterns were designated as representing the
behavioral states previously described in the
literature, and the percentage of time a fetus
spent in any predefined state was computed.
This measure represents the degree to
which fetuses displayed concordance, as opposed to discordance, of state parameters.
Infant Temperament
Infant temperament at 3 and 6 months
was assessed by the Infant Characteristics
Questionnaire (ICQ; Bates, Freeland, &
Lounsbury, 1979), which was administered
through the mail. Data were quantified in
four factors of Fussy-Difficult, Unadaptable,
Dull, and Unpredictable based on scoring
procedures developed through factor analysis by Bates et al. (1979). Higher scores indicate greater fussiness or difficultness, unadaptability (i.e., to new persons and
situations), dullness (i.e., lack of emotional
tone), and unpredictability (i.e., lack of regularity in eating and sleeping habits). Two additional questions were added to elicit targeted information concerning infant state
and activity level. These were (a) "In general, how active is your baby? That is, when
you put your baby down, or when you're
holding your baby, how much does the baby
squirm and wriggle around?" Responses
were based on a scale of 1 (low active) to 7
(very active), and (b) "How often does your
baby wake up during the night?"; responses
were open-ended. In addition, at each age,
parents reported the approximate proportion
DiPietro et al. 2571
of the infant's diet that was composed of
breast milk.
Analysis Strategy
Cross-time correlation matrices of the
repeated measures for each of the six fetal
variables (FHR, FHR variability, fetal activity level and periodicity, state organization,
and reactivity) and for infant temperament
ratings were constructed. The patterning of
significant correlations was used to evaluate
the apparent stability during gestation of
each variable. In order to reduce the number
of ainalyses, the final regressions were based
only on the 36-week fetal assessment. Fortyfive percent (n = 14) of the study participants delivered prior to their final visit at
38/39 weeks, so data from the last recording
were not used due to the high degree of
missing data. A separate standard multiple
regression which included all 36-week fetal
variables was conducted for each dependent
measure (four ICQ factors, activity level, and
night wakings) at both 3 and 6 montbs. Any
covariate wbicb was significantly correlated
(p < .05) with any dependent measure was
forced into the equation at the first step; all
fetail variables were then entered at the next
step. Three subjects did not have reactivity
datii at 36 weeks because they did not display the requisite 2-min period of low variability in heart rate; these missing data were
replaced by 32-week values for these cases
in order to preserve degrees of freedom.
Whenever significant relations between fetal measures at 36 weeks and infant temperament were detected, additional correlational
analyses were conducted to determine tbe
earliest age in gestation at which this relation could be observed. Tbese results are reported following each regression.
Results
Stability of Fetal Measures
Correlation matrices for each ofthe fetal
measures during gestation are presented in
Tables 1 through 4. Correlations for both
FHR and FHR variability are significant between most pairs of gestational ages (Table
1). The overall means of all the correlations
in the matrix for FHR and FHR variability
are r = .39 and r =.43, respectively. Although the highest correlations are between
pairs closest in time (i.e., 1 month apart), this
is not always the case. The patterns of correlations in this matrix suggest that both FHR
and variability are fairly stable during the
period of gestation studied.
Fetal activity level (Table 2) also appears to be most stable between closer assessment periods, and after 32 weeks. Earlier in gestation there are significant pairs of
correlations (e.g., between 24 and 32 weeks),
but tbe magnitude of the correlations is
small. Stability in fetal activity periodicity is
not evident until 32 weeks, although again
there were significant associations scattered
throughout the matrix at earlier ages.
Cross time correlation coefficients for
the higher order processes represented by
fetal state and reactivity (Tables 3 and 4) are
much smaller than those for fetal heart rate
and activity measures. The proportion of
time spent in organized fetal states did not
show evidence of stability until 36 weeks.
Fetal reactivity did not display any consistent pattern indicative of stability of this
measure. Because fetal reactivity consisted
of two components—size and duration of response—separate matrices were conducted
to determine whether stability existed in
TABLE 1
INTERCORHELATIONS OF F E T A L H E A R T R A T E AND F E T A L HEART RATE VARIABILITY
DURING G E S T A T I O N
GESTATIONAL AGE (Weeks)
GESTATIONAL
AGE
20
24
28
32
36
38-39
20
24
28
32
36
38-39
...
58
46
24
03
61
.61
...
.53
.40
.30
.53
.56
.54
...
.60
.35
.55
.28
.43
.39
...
.43
.32
.26
.38
.56
.48
•••
.48
.15
.16
.34
.25
.52
NOTE.—rs above the diagonal are for FHR; rs below the diagonal are for FHR variability,
ns for pairs in the first five rows and columns = 31; correlations 3= .30 are significant at the .05
level or greater, ns for the last column and row = 17; correlations s= .41 are significant at the
.05 level or greater.
TABLE 2
INTERCORRELATIONS O F FETAL ACTIVITY LEVEL AND PERIODICITY
DURING GESTATION
GESTATIONAL AGE
GESTATIONAL
AGE
20 ..
24
28
32
36
38-39
20
...
...
...
...
...
.09
.19
.53
.20
.15
24
28
.30
.27
.11
.18
.24
.18
.44
.23
.09
.50
(Weeks)
32
36
38-39
35
55
.05
.26
.47
.45
.34
.28
.16
.48
.67
44
.64
.37
NOTE.—rs above the diagonal are for fetal activity level; rs below the diagonal are for fetal
activity periodicity, ns for pairs in the first five rows and columns = 31; correlations '» .30 are
significant at the .05 level or greater, ns for the last column and row = 17; correlations s .41
are significant at the .05 level or greater.
TABLE 3
INTERCORKELATIONS O F FETAL STATE ORGANIZATION DURING GESTATION
GESTATIONAL AGE (Weeks)
GESTATIONAL
AGE
20
20
24
28
32
36
38-39
•••
.27
.25
.05
.04
-.09
.00
-.12
-.08
.09
-.39
-.27
-.37
.16
.49
.39
24
28
32
36
NOTE.—ns for pairs in the first five rows and columns = 31; correlations s .30 are significant
at the .05 level or greater, ns for the last column and row = 17; correlations ^ .41 are significant
at the .05 level or greater.
TABLE 4
INTERCOBRELATIONS O F FETAL REACTIVITY DURING GESTATION
GESTATIONAL AGE
GESTATIONAL
AGE
20
24
32
20
(Weeks)
24
28
32
36
38-39
-.11
(23)
.50*
(23)
-.20
(28)
.23
(19)
.01
(24)
''3
(24)
.06
(22)
.27
(26)
17
(27)
.48*
(22)
-.18
(13)
.20
(15)
34
(14)
.05
(14)
.29
(13)
NOTE.—Due to varying amounts of missing data at each gestational age, analyses were
conducted with pairwise deletions; ns per pair are provided in parentheses.
*p< .01.
DiPietro et al.
one of these domains. Significant stability
was not detected for either.
Infant Temperament
One subject did not return the temperament questionnaire at either time, two others failed to complete the 6-month questionnaire; thus the ns for the 3-month and
6-month analyses are 30 and 28, respectively. The 3—6-month within-factor correlations are: Fussiness, r = .80; Unadaptability, r = .66; Dullness, r = .49;
Unpredictability, r = .63; Activity Level, r
= .58; and Night Wakings, r = .62.
Mean values for the independent and
dependent measures for the sample are presented in Table 5. The following variables
were explored as potential covariates which
might affect maternal perceptions of infant
temperament or infant temperament itself:
infant sex and birthweight, method of feeding at 3 and 6 months (proportion of breast
milk in diet), parity (primiparous vs. multiparous), maternal age, and maternal education. Maternal age, parity, infant birthweight, or sex were not significantly
correlated with any dependent measure. At
3 months only, there were marginal correlations {p < .10) between the amount of breast
milk an infant received and three ofthe four
ICQ factors (rs were .26, .25, and .24, respec-
tively, for fussiness, unadaptability, and unpredictability); this measure was included as
a covariate in these equations because ofthe
consistency ofthe relation. At 3 months, 48%
of infants were exclusively fed with breast
milk, wbile 32% received no breast milk.
Maternal education was significantly correlated with reports of both infant activity and
night waking at 6 months only (rs = .33 and
.32); more educated women reported their
infants as more active and awake more often
at night. Maternal education was included
in the regression for these variables.
Tables 6 through 11 present the results
ofthe regression analyses at 3 and 6 months
for each dependent measure. Data are presented for the unstandardized (B) and standardized regression coefficients (p), t test
values and significance levels, and both
zero-order (r) and partial correlations (pr) for
each independent fetal variable. Because
shared variance among independent measures can obscure associations between individual measures and the dependent variable, the partial correlations help in the
interpretation of the associations between
the fetal and infant measures by removing
the variance distributed among the fetal
measures. Multiple Rs, R^, and F values are
provided at each step in the equation (i.e..
TABLE 5
MEANS AND VARIABILITY FOR INDEPENDENT AND DEPENDENT MEASURES
Mean
SD
Range
140.62
5.77
9.08
3.29
.89
44.49
7.03
1.41
7.37
2.38
.13
71.54
125.7-152.3
3.4-9.1
.9-26.8
0-8
.53-1.00
0-280.8
Infant 3-month measures (n = 30):
Fussy-Difficult
Unadaptability
Dullness
Unpredictability
Activity level
Night waking
16.47
8.70
8.70
8.20
5.20
1.03
5.44
3.70
2.31
3.20
1.35
.93
9-31
4-17
4-14
3-13
2-7
0-4
Infant 6-month measures (n = 28):
Fussy-Difficult
Unadaptability
Dullness
Unpredictability
Activity level
Night waking
16.04
8.71
7.96
7.54
5.57
1.04
5.22
4.02
2.05
2.60
1.20
1.02
9-27
4-20
4-11
4-13
4-7
0-3
36-week fetal measures (n = 31):
Fetal heart rate (FHR)
FHR variability
Fetal activity leveP
Fetal activity periodicity
State organization
Reactivity''
2573
• These measures are based on composite scores. Activity level = number x duration of
all movements; reactivity = magnitude x duration of response to the vibratory stimulus.
2574
Child Development
for the initial entry of covariates, if any, and
for the fetal measures combined).
Infant fussiness.—The overall F values
for botii the 3 and 6 month regressions were
significant, and the fetal measures accounted
for 37% and 43% of the variance in infant
fussiness, respectively. These results are
presented in Table 6. Fetal activity level and
periodicity were significantly correlated
with both 3- and 6-montb fussiness, indicating that more active fetuses, who cycled less
often between quiet and active periods,
were more fussy. However, only fetal activity level remained significant in the regression at 6 months. At 3 months, inspection
of the partial correlations reveals that fetal
reactivity to stimuli was the best single predictor of fussiness; fetuses who displayed a
greater response to the stimulus were also
the most fussy/difficult. This relation did not
persist at 6 months.
Prior to 36 weeks, correlations among
fetal activity level, reactivity, and 3-month
fussiness were not significant, although the
observed relation with periodicity was evident a month earlier, at 32 weeks (r = - .32).
Associations between activity level and 6month fussiness were in the same direction
beginning at 28 weeks altbough not significant (24 week r = .29, 28 week r = .27), and
the relation with periodicity also was evident at 32 weeks.
Infant Unadaptability.—The overall F
for Unadaptability was marginally significant at 3 months and significant at 6 months
(Table 7). At 3 months, the single best predictor was activity periodicity, witb greater
unadaptibility associated with less periodicity. This relation was no longer evident at
6 months once the shared variance among
measures was partialed, but overall activity
level remained positively associated with
greater unadaptability. The correlations between activity level and unadaptability were
significant as early as 24 weeks' gestation.
In addition, poorer state organization was
correlated with 6-month Unadaptability, although the t for this variable as entered in
the regression did not attain significance.
There was a significant zero-order correlation between FHR and Unadaptability, but
this relation disappears in the partial correlations. However, significant relations between both 3 and 6 month Unadaptability
and FHR were observed from 32 weeks (rs
= .44 and .33, respectively).
Infant Dullness.—The ICQ factor
"Dull" was negatively predicted by fetal activity periodicity at both 3 and 6 months (Table 8). At both ages, infants who were rated
TABLE 6
PREDICTION OF INFANT FUSSINESS FROM 36-WEEK FETAL MEASURES
B
Dependent measure: Fussy-DifHcult
(3 months):
Infant feeding method
.04
.34
Multiple R = .26; R^ = .07; F(l, 28)
Fetal heart rate
7.01
9.21
FHR variability
-.53
-.14
Activity level
.14
.19
Activity periodicity
-.57
-.25
State organization
-8.20
-.20
Reactivity
03
.49
Multiple R = .66; R^ = .44; F(7, 22)
Dependent measure: Fussy-Difficult
(6 months):
Fetal heart rate
-.14
-.19
FHR variability
-.69
-.19
Activity level
.42
.60
Activity periodicity
—.23
—.11
State organization
—3.36
—.09
Reactivity
2.27
.03
Multiple R = .65; R^ = .43; F(6, 21)
* p< .10.
*p< .05.
**p< .01.
*** p < .001.
pr
1.92+
•• 2 . 1 1
.04
-.77
.76
1.27
1.03
2.50*
= 2.49*
-.91
1.01
2.49*
-.54
-.43
.16
= 2.59*
.26
.23
-.05
.52**
-.36*
-.18
.32*
.18
-.20
.60***
-.37*
-.24
.12
.38*
.01
-.16
.16
.26
-.21
.39*
-.19
-.21
48**
-.12
-.09
.03
TABLE 7
PREDICTION OF INFANT UNADAPTABILITY FROM 36-WEEK FETAL MEASURES
B
B
t
r
Dependent measure: Unadaptability
(3 months):
Infant feeding method
02
.25
1.35
Multiple R = .25; R^ = .06; F(l, 28) = 1.81
Fetal heart rate
-.03
-.05
-.23
.03
FHR variability
08
.16
Activity level
12
.25
.94
Activity periodicity
-.61
-.40
-1.91
State organization
-3.08
-.11
-.54
Reactivity
-8.06
-.15
-.76
Multiple R = .62; R^ = .
'(7, 22) = 1.96+
Dependent measure: Unadaptability
(6 months):
Fetal heart rate
-1.48
-2.66
-.01
FHR variability
-.52
-.19
-1.01
Activity level
22
.42
1.78
Activity periodicity
-.13
-.07
-.39
State organization
-8.94
-.30
-1.52
Reactivity
-9.59
-.17
-.88
Multiple fi = .67; fi^ = .45; F(6, 21) = 2.89*
.25
pr
.28
26
08
45**
47**
19
12
-.05
.03
.20
-.38*
-.11
-.16
34*
18
54**
34*
47**
15
.00
-.22
.36*
-.08
-.31*
-.19
+ p < .10.
*p< .05.
** p < .01.
TABLE 8
PREDICTION OF INFANT DULLNESS FROM 36-WEEK FETAL MEASURES
B
t
Dependent measure: Dullness
(3 months):
Fetal heart rate
-.03
-.09
-.43
FHR variability
-.33
-.21
-1.08
Activity level
-.04
-.12
-.50
Activity periodicity
-.54
-.57
-2.75**
State organization
-.44
-.03
-.13
Reactivity
5.33
.16
.82
Multiple R = .57; fi^ = .33; F(6, 23) = 1.86
Dependent measure: Dullness
(6 months):
Fetal heart rate
08
.28
1.34
FHR variability
-.24
-.17
-.88
Activity level
-.02
-.09
-.36
Activity periodicity
-.42
-.50
-2.48*
State organization
—1.74
.12
.56
Reactivity
1.97
.07
.34
Multiple fi = .64; fi^ = .41; F(6, 21) = 2.44*
* p< .10.
* p < .05.
**p< .01.
*** p < .001.
pr
.04
-.25
.14
- .50**
.08
.08
.36*
-.22
.27
-.58***
.02
.04
-.09
-.22
-.10
- .50**
-.03
.17
.28
-.19
-.08
- .48**
.12
.07
2576
Child Development
as lacking in emotional tone displayed the
most invariant patterns of fetal activity. Because this was the only significant fetal predictor at 3 months (note the unchanging partial correlation), the overall F for the
equation did not attain significance. At 6
months, higher fetal heart rate was also associated with infant Dullness, but most of the
variance appetirs to be shared with activity
periodicity. However, while earlier correlations between Dullness and activity periodicity were not significant prior to 36 weeks,
there were significant associations between
this factor and fetal heart rate at each age
from 20 weeks (rs range from .30 to .57).
Confirmatory regressions indicated that
FHR was the only significant predictor of
the Dull factor at 24, 28, and 32 weeks (ts =
3.52, 1.98, and 3.17, respectively).
Infant Unpredictability.—Sixty percent
of the variance in infant Unpredictability at
3 months was accounted for by the fetal measures (Table 9), a finding that was carried
by the associations with activity level and
periodicity. High levels of activity and less
periodicity were associated with greater infant unpredictability. The association with
activity level, but not periodicity, was significant beginning at 32 weeks (r — .45).
However, at 6 montbs tbese associations
were diminished, and the overall F for the
equation was not significant. Zero-order correlations for activity level and periodicity
did not remain significant when the contribution of other variables was partialed. At 3
and 6 months, fetal heart rate displayed a
similar correlation with Unpredictability,
but its significance in a partial correlation
was retained only at 6 montbs. Significant
zero-order correlations between FHR and 6month Unpredictability commenced at 24
weeks' gestation.
Activity level.—The overall F's for the
equations approached, but did not attain,
significance at 3 and 6 months, although the
fetal measures were associated with 38%
and 31% of the variance in infant outcomes,
respectively (Table 10). Altbougb the
amount of variance in infant temperament
predicted by the fetal measures together was
only marginally different from zero, the patterning of individual fetal measures warrants
further scrutiny because of specific predictions concerning fetal activity level alone. At
both ages, fetal heart rate and activity level
were significantly associated with infant activity levels. The zero-order correlations for
FHR were not significant, but the t value
and partial correlations were, suggesting a
masking effect of the other fetal measures on
TABLE 9
PREDICTION OF INFANT UNPREDICTABILITY FROM 36-WEEK FETAL MEASURES
B
t
Dependent measure: Unpredictability
(3 months):
Infant feeding method
-.01
.22
1.58
Multiple R = .24; R = .07; F(l, 28) = 1.74
Fetal heart rate
04
.09
.55
FHR variability
06
.03
.20
Activity level
24
.55
2.89**
Activity periodicity
—.40
-.30
-1.98+
State organization
2.49
.10
.69
.05
Reactivity
2.43
.36
Multiple H = .82; R^
.67; F(7, 22) == 6.39***
Dependent measure: Unpredictability
(6 months):
.38
1.69
Fetal heart rate
14
FHR variability
-.12
-.07
-.33
Activity level
.10
.30
1.14
-.05
-.22
Activity periodicity
-.05
.26
1.15
State organization
4.87
.08
.36
Reactivity
2.84
Multiple R = .57; R = .33; F(6, 21) = 1.72
+ p < .10.
* p < .05.
** p < .01.
*** p < .001.
pr
.24
.32*
.46**
-.01
.74***
-.58***
-.13
.17
.52**
-.39*
.15
.08
.45**
-.06
.43**
-.32*
.35*
-.07
.24
-.05
.00
.17
.24
.08
.12
.04
DiPietro et al.
2577
TABLE 10
PREDICTION OF INFANT ACTIVITY LEVEL FROM 36-WEEK FETAL MEASURES
B
t
Dependent measure: Activity level
(3 months):
-.43
Fetal heart rate
- .08
FHR variability
29
.31
.50
Activity level
09
-.08
Activity periodicity
—.04
-.20
State organization
—2.02
.03
Reactivity
6.20
Multiple fi = .61;
= .38; F(6, 23)
Dependent measure: Activity level
(6 months):
.35
Maternal education
.22
Multiple fi = .33;fi2-- .11; F(l, 26)
Fetal heart rate
-.07
-.44
FHR variability
-3.21
-3.92
.49
Activity level
.08
.09
Activity periodicity
.05
State organization
-2.27
-.26
Reactivity
2.15
.13
Multiple fi = .65;
= .43; F(7> 20)
pr
-2.03*
1.65
2.07*
-.40
-1.03
.17
= 2.31+
.00
.31*
.40**
.12
.32*
.23
.39*
.32*
.40**
-.08
-.21
.03
1.95+
= 3.17+
-2.03*
-.02
2.30*
.45
-1.21
.63
= 2.11+
.33*
.40**
.03
.11
.37*
.02
.37*
.15
-.41**
.00
.41**
.10
-.26
.14
+ p < .10.
* p < .05.
** p < .01.
FHR. The FHR variability was minimally
associated with 3-month activity level only,
but the t was not significant. None of the
relations with infant activity level was consistently significant prior to 36 weeks.
Night wakings.—Fetal measures significantly predicted the amount of night
wakings reported by parents at 3 months
(Table 11). In particular, fetuses with poorer
state organization and less activity periodicity woke more often. This relation did not
persist at 6 months, although the zero-order
correlations were significant and in the same
direction. Inclusion ofthe significant covariate of maternal education On the first step
accounted for the greatest portion of the
shared variance. Consistent relations with
fetEil measures prior to 36 weeks with night
waking could not be identified.
Fetal activity patterns.—During data
collection we observed an uncommon yet
striking pattern of fetal activity, characterized by at least 3 min of uninterrupted bursts
of extremely vigorous high amplitude movement which was coded as FM pattern 4. A
subset of eight subjects displayed this pattern once for some portion of the 36-week
recording (M episodes = 4.0). Results of t
tests comparing infant temperament of this
group to fetuses who did not display this pat-
tern yielded significant or marginally significant differences in four of the six infant
measures at 3 months and all of the infant
measures at 6 months. In all tests, high fetal
activity was associated with more difficult
temperament. Means and t test results are
presented in Table 12. Inverse associations
between difficultness and the display of periods of extreme quiescence were not found.
Stability during Gestation
Finally, exploratory analyses were conducted to determine whether individuals
who were stable on each fetal measure during gestation were more likely to display
certain temperament characteristics as infants. To do this, we attempted to identify
fetuses who were either consistently above
or below the mean for at least four of the
five recordings from 20 through 36 weeks.
Defined this way, there were insufficient
cases of individuals who could be classified
as stable for the variables of activity periodicity, state regulation, and reactivity. Small
subgroups of fetuses could be identified on
the remaining measures, permitting exploratory group comparisons between consistently high and consistently low scorers. Fetuses who displayed high FHR throughout
gestation (n = 7) were more Unpredictable
at both 3 and 6 months, t{14) = -2.57, p <
TABLE 11
PREDICTION OF INFANT NIGHT WAKING FROM 36-WEEK FETAL MEASURES
B
p
t
Dependent measure: Night waking
(3 months):
Fetal heart rate
-.02
-.12
-.63
FHR variability
-.05
-.08
-.48
Activity level
4.45
3.58
.02
Activity periodicity
-.22
-.58
-3.20**
State organization
-2.80
-.41
-2.30*
Reactivity
2.16
.16
.94
Multiple R = .69; R^ = .48; F(6, 23) = 3.58**
Dependent measure: Night waking
(6 months):
Maternal education
21
.40
2.04*
Multiple R = .31; R^ = .10; F(l, 26) = 2.86
Fetal heart rate
-.01
-.07
-.32
FHR variability
-.08
-.12
-.55
Activity level
04
.28
1.04
Activity periodicity
-.07
-.19
-.85
State organization
1.03
.14
.61
Reactivity
2.94
.21
.94
Multiple R = .56; R^ = .32; F(7, 20) = 1.32
r
pr
.25
-.04
.42**
-.58***
-.38*
.12
-.13
-.10
.00
- .56***
- .43**
.19
.31*
.41*
.16
-.07
.34*
-.32*
-.03
.20
-.07
-.12
.23
-.18
.13
.21
+ p < .10.
* p < .05.
** p < .01.
*** p < .001.
TABLE 12
INFANT TEMPERAMENT IN HIGHLY ACTIVE FETUSES
HIGHLY ACTIVE
FETUSES
M
Infant 3-month measures
Fussy-Difficult
Unadaptability
Dullness
Unpredictability
Activity level
Night waking
Infant 6-month measures
Fussy-Difficult
Unadaptability
Dullness
Unpredictability
Activity level
Night waking
+ p < .10.
* p < .05.
** p < .01.
*** p < .001.
OTHER
FETUSES
SD
M
7.1
3.5
1.2
2.4
.9
1.3
14.9
7.5
8.3
6.9
5.0
.9
6.6
4.8
1.0
2.4
1.1
1.3
14.1
7.4
7.5
6.9
5.3
53
.8
(n = 8)
20.7
12.0
9.7
11.9
5.6
1.5
(n = 22)
(n = 7)
21.7
12.7
9.4
9.4
6.3
1.6
SD
3.8
3.0
2.5
2.3
1.5
.7
2.92*
3.46**
1.54
5.25***
1.04
1.72+
2.9
2.7
2.1
2.3
1.1
1 1
.8
4.25***
3.68***
2.37*
2.41*
1.91 +
1.69+
(n = 21)
DiPietro et al.
.05, and t{12) = -3.62, p < .01, and more
Unadaptable at 6 months, t(12) = -2.13, p
< .05, than were those with consistently low
FHR (n = 9). There were no significant associations between infant temperament and
stability in FHR variability. Consistently
high active (n = 7) versus consistendy low
active fetuses (n = 10) were more Unadaptable at 3 and 6 months, *(15) = -2.57, p <
.05, and *(13) = -2.31, p < .05, and more
Unpredictable at 3 months, t{15) = -2.43,
p < .05.
Discussion
The results of this study indicate tbat
behavioral and physiologic characteristics
that have been associated with temperament
first demonstrate levels of stability characteristic of traits during gestation. The sequencing of the gestational age at which
stability is manifest parallels the neuromaturational ontogeny of that characteristic.
The stabilization of autonomic (i.e., heart
rate) measures first, followed by motor behavior and state organization parallels the
developmental hierarchy of neuromaturation applied to preterm infants (Als, 1982).
The magnitude of the correlations observed
for stability in FHR and FHR variability are
comparable to those reported recently for
preterm infants (DiPietro et al., 1994). Antenatal stability in motor activity had been reported in two previous studies. Tbe first reported consistency in the duration of motor
activity from the second trimester to the
third trimester in 12 fetuses visualized
through real time ultrasound (deVries, Visser, & Prechtl, 1988). In the second, daily
maternal report of fetal activity was determined to be relatively stable from 28
through 39 weeks' gestation (Eatdn & Saudino, 1992), although intrafetal correlations
are not presented so direct comparisons with
the current data are not possible. Activity
level is tbe most pervasive dimension of
temperament across taxonomies and one of
the most robust (Hubert et al, 1982). Including data from the current study, the origin of
activity level as a stable individual difference before birtb has now been confirmed
using three different methodologies to study
fetail activity.
We were unable to document antenatal
stability in reactivity to an extrauterine stimulus, suggesting that this is not a reliable
individual difference prior to birtb. However, of all the neurobebavioral measures,
reactivity to stimuli tbat are extrauterine in
origin is tbe most difficult to measure well.
2579
Several factors may have limited our ability
to detect individual differences in reactivity
effectively. For example, responsiveness to
a more intense stimulus has been shown to
be partially dependent on fetal state during
application (Devoe, Murray, Faircloth, &
Ramos, 1990). Although the vibroacoustic
stimulus in this study was applied during a
period of low FHR variability, we did not
control for fetal state or activity. In addition,
intrauterine factors may affect fetal detection
of the stimulus, such as placental position
relative to the stimulus and amniotic fiuid
volume. The impact of such factors requires
further investigation before instituting
methodologic or statistical controls. Finally,
our efforts to quantify FHR or activity
change from a fiuctuating baseline presents
computational challenges that may not have
been most effectively handled. Because reactivity has emerged as a core construct and
a productive dimension of investigation for
botb temperament and psychobiologic research, we do not advocate dismissing reactivity as a measure in future fetal research.
However, careful methodologic studies on
the effect of intrauterine and extrauterine
factors on both fetal stimulus detection and
responsiveness must be conducted before
any relation between antenatal reactivity
and subsequent development can be conclusively determined.
Individual differences in many features
of fetal functioning predicted maternal reports of infant temperament, some originating as early as 24 weeks' gestation. The relations were quite robust: fetal neurobehavior
at 36 weeks accounted from 32% to 60% of
the variance for the ICQ temperament scale,
infant activity level, and night waking, at 3
months and between 22 and 45% at 6
months. Maternal and infant covariates did
not appreciably affect tbese findings. Most
of the attributable variance in predicting tbe
four ICQ factors is associated with measures
of fetal motility: fetal activity level and activity periodicity. Although the significance
levels of the partial correlations vary across
measures and sometimes differ between 3
and 6 months, in general, higher activity is
associated with increased difficultness, unadaptability, and unpredictability. Conversely, greater periodicity (i.e., sborter
bouts of activity interspersed with inactivity), was associated with lower scores on
these factors, as well as the Dullness factor.
Thus higher fetal activity and/or fewer episodes of cycling through activity and quiescence are associated with greater infant
2580
Chad Development
negative responsivity and poorer selfregulation, as well as better emotional tone
in general. Hyperreactivity, including low
threshold and high intensity, as well as hyporegulatory capacities underlie these temperament characteristics. Our findings suggest that measures of fetal motility may
refiect individual differences in regulatory
processes in general. In infants, activity is
considered to be a regulator of stimulation
(Fox & Stifter, 1992), and such a function
may be applicable to the fetus as well. This
interpretation is strengthened by the identification of a subgroup of fetuses who displayed episodes of extreme activity at 36
weeks. With the exception of Dullness at 3
months, this pattern of fetal activity was
strongly predictive of higher scores on each
of the ICQ factors at both 3 and 6 months.
Using the Fussy — Difficult factor at 6
months as an example, all infants (n = 5)
who scored more than 1 SD above the mean
had displayed at least three episodes (i.e., 9
min) of extreme activity at 36 weeks. The
sensitivity and specificity of this single pattern of high activity in the prediction of high
fussiness at 6 months are 100% and 91%, respectively.
Fetal heart rate at 36 weeks did not predict any ICQ factor. However from 24
through 32 weeks, fetuses who had higher
heart rates were those who were rated as
having less emotional tone (Dullness factor)
at 6 months (at 36 weeks the unadjusted correlation was also significant). This finding is
intriguing because it is consonant with
cross-sectional data collected on infants. At
4 months, infant heart rate has been reported
to be negatively associated with maternal report of infant emotional responsiveness
(Stifter & Fox, 1990). In addition, we found
fetal heart rate to be a significant predictor of
infant activity level at both ages, with faster
heart rate associated with lower activity
once the other fetal measures were controlled. However, botb findings are inconsistent with recent reports of positive relations
between fetal and 2-week postpartum heart
rate and greater negative reactivity to novel
and arousing stimuli at 4 months (Snidman
etal., 1995). Our subgroup analysis based on
individual consistency determined that fetuses with consistently higher heart rates
throughout gestation were also more likely
to be rated as Unpredictable at 3 and 6
months, and Unadaptable at 6 months.
These results are consistent with the unadjusted correlation coefficients based on 36week data alone. The characteristics in-
cluded in these ICQ factors involve
tolerance to novelty and may have direct relevance for the Snidman et al. (1995) results.
The general lack of significant findings
with fetal heart rate variability was unexpected because of the infant literature supporting a relation with several dimensions of
difficult temperament (DeCangi et al., 1991;
Fox, 1989; Porges et al., 1994). However,
heart rate variability in the fetus is infiuenced by maternal factors, including appraisal of stress and maternal age, in ways
that other fetal measures are not (DiPietro
et al., 1996, in this issue). Further, although
most infant studies of cardiac patterns limit
data collection to one or two relatively quiescent states (e.g., quiet alertness or active
sleep), we quantified this measure across the
entire recording. Because bursts of fetal
movement tend to be brief and scattered
throughout the entire recording, we did not
limit FHR data to periods of similar activity
or quiescence across subjects for methodologic reasons. It is possible that potential associations between variability and infant
temperament might be masked by this decision. That is, for highly active fetuses, FHR
variability data were more often collected
during periods of motor activity than was the
case for less active fetuses. Although fetal
movement tends to be associated with
higher FHR variability, we found no consistent relations between the amount that a fetus moved during a recording and FHR variability (correlations at each successive
gestational age were: r = —.04, .30, ^ . 2 1 ,
.18, .05, and -.10). Thus, although we do
not believe such an association systematically affected our results, analysis of FHR
variability data collected during a single
state or activity pattern would further understanding of the relation between cardiac patterns and temperament, independent of
other behavioral parameters.
Fetal reactivity was unsuccessful in predicting infant temperament, despite the theoretical commonalities between the two
concepts. Additional post hoc analyses conducted on the separate components of this
measure (response magnitude and duration),
failed to yield any significant associations
with temperament. The single significant regression finding, that of a positive relation
between fetal reactivity and infant fussiness
at 3 months, illustrates the value of using a
multivariate approach to the investigation of
fetal neurobehavior and temperament. Without it, the relevance of this single association
might be overstated. However, the limita-
DiPietro et al.
tions in measuring fetal reactivity have been
previously discussed.
Prediction of the two additional infant
measures, activity level and night waking,
Was confounded by maternal education at 6
montbs. Despite this, the significant associations between fetal and infant activity level
Were of a Similar magnitude at 3 and 6
months (partial correlations = .40 and .41,
respectively). These data are the first to
show continuity between antenatal and postnaital activity level; other efforts have failed
to find a relation (Eaton & McKeen, 1987;
Shadmi et al., 1986). Previous studies had
relied on fetal activity data generated
through maternal perception of fetal movement which is of limited utility because
women usually do not detect tbe sinaller, localized movements which predominate fetal
activity (Johnson, Jordan, & Paine, 1990).
Finally, infant night waking was negatively associated with fetal state organization
and activity periodicity in utero. Fetuses
with more mature state regulation and more
periodic bouts of quiescence and activity at
36 weeks woke less often when they were 3
months old. This is the only measure for
which fetal state organization was a significant individual predictor in the regressions
but is consistent with our original hypothesis. However, by 6 months this relation was
no longer observed.
We have provided evidence that stable
individual differences in fetal cardiac patterns, activity level, and to a lesser degree,
stiite, do exist. The interpretation ofthe significant predictive relations between fetal
characteristics and later maternal report of
infant temperament are not so straightforward. Although we are tempted to conclude
that these data provide clear support for fetal
origins of infant temperament:, our reliance
on maternal report of temperament leaves at
least one other interpretation possible. Results of a series of studies in which temperament scales were administered during pregna^ncy indicate that there is stability in
pregnant women's responses to these questionnaires from pregnancy to infancy (Wolk,
Zeanah, Garcia Coll, & Carr, 1992; Zeanah,
Keener, Stewart, & Anders, 1985), although
the validity of the response demands associated with this type of task has been challenged (Carey & McDevitt, 1985). If women
do develop an image of the fetus during
pregnancy and maintain those attributions
through the neonatal and infant periods, regardless ofthe infant's actual behavior, our
2581
data would suggest that their projections are
based on actual fetal behavior. Ultimate interpretation of the results of this study,
which are among the first to establish the
antenatal origins of stable fetal characteristics and consistency with later temperament,
require replication and elaboration to include laboratory based assessments of infant
temperament, botb of which are currently
underway.
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