Cardiac-somatic integration: An index of visual attention

Cardiac-somatic integration: An index of visual attention

INFANT BEHAVIOR AND DEVELOPMENT 10, 493-500 (1987) Cardiac-Somatic Integration: An Index of Visual Attention JOSEPH M. BYRNE Dalhousie Universi...

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INFANT

BEHAVIOR

AND

DEVELOPMENT

10,

493-500

(1987)

Cardiac-Somatic Integration: An Index of Visual Attention JOSEPH M. BYRNE Dalhousie University School of Medicine lzaak Walton Killam Hospital for Children DAPHNE

J. SMITH-MARTEL

Izaak Walton Killam Hospital for Children Eighteen 15.week-old. normol full-term infants were presented with photographic slides of o human facial expression. The infant’s heart rate, body movement, and visual attention were recorded simultaneously. The results showed that heort rote and body movement were significantly correlated during visual attention but not during inattention. Bath heart rate and body movement decelerated significantly when the infants visually ottended to the target stimulus. The results ore discussed with reference to cardiac-somatic integration in early infancy and its implication OS a possible index of attention.

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integration activity

visuol attention infants

One of the more compelling questions in adult psychophysiology has been the functional relationship between autonomic (notably, heart-rate) and behavioral response systems (Lacey & Lacey, 1974; Obrist, 1976). Research has shown that adults have a strong cardiac-somatic relationship; in some cases, it may extend to rough equivalence among response systems in their sensitivity to various stimulus parameters (e.g., Morse, Leavitt, Miller, & Romero, 1976). It has been suggested that cardiac-somatic integration is a fundamental dimension of attention. Both cardiac and behavioral responses have been used individually to infer infant attention to stimuli presented in a variety of modalities (see Berg & Berg, 1979, and Olson & Sherman, 1983, for reviews). However, few studies This research was supported by Federal Research Grant No. 6603-l 179-X awarded to Joseph M. Byrne from the National Health Research Development Program, Ottawa. Canada. Portions of this paper were presented at the 47th Annual Meeting of the Canadian Psychological Association, Toronto, June, 1986. The authors wish to thank the infants and their parents for their participation, William Hayes for computer programming consultation, Ken Magee and Norman Knickle for biomedical engineering consultation, and Helene Whitford and Christene Horton for secretarial assistance. Special thanks go to the Grace Maternity Hospital and the Nova Scotia Hearing and Speech Clinic for their continued assistance in recruiting infants. Correspondence and requests for reprints should be sent to either author at the Department of Psychology, Izaak Walton Killam Hospital for Children, 5850 University Avenue, Halifax, Nova Scotia, Canada B3J 3G9. 493

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have examined these responses jointly in order to determine their relationship to infant attention. Most studies in which both responses have been recorded have focused on the issue of whether somatic activity had a nonfacilitative effect on a major index of attention, the cardiac deceleratory response. For example, Nelson, Clifton, Dowd, and Field (1978) found that sucking activity attenuated the newborn’s cardiac deceleratory response, and recommended controlling for sucking if cardiac activity was the major dependent measure in a particular study. Pomerleau and MaIcuit (1980) found that young infants (I 3 months) showed a cardiac deceleratory response while attending to a threedimensional object but older infants (L 5-6 months) exhibited a cardiac acceleratory response, possibly reflecting the older infants’ preparedness or intention to reach for the object. The authors made the important distinction between “passive” and “active” information-processing demands of a task (e.g., threedimensional toy) and the degree of perceptual-motor ability; events prone to elicit a motor response (reaching) will more likely elicit heart-rate acceleration. Morrongiello and Clifton (1984) recently found that newborns were capable of cardiac deceleration to auditory stimuli, but only in the absence of headturning or low somatic activity. In contrast, Smonth-olds demonstrated cardiac deceleration irrespective of the presence or absence of head movement, although even for the Smonth-olds, the cardiac deceleratory response was significantly less than observed during no head-turn. This may suggest tentatively that with development, cardiac-somatic systems become more independent even during attention to certain passive tasks (e.g., Pomerleau & Malcuit, 1980). Morrongiello and Clifton encouraged the simultaneous recording of cardiac and behavioral measures so as to provide a convergent index of infant attention. The importance of recording both cardiac and behavioral measures is highlighted in a study by Miller and Byrne (1983). They found full-term newborns in a light sleep state had a moderate degree of cardiac-somatic integration during the presentation of speech sounds; heart-rate acceleration and increased body movement were observed with stimulus onset. However, although heart rate was differentially responsive to various acoustic parameters, general body movement was not. In recent years, there has been an appreciable increase in the study of infant movement, its level, rate, and temporal pattern (e.g., Korner et al., 1985; Robertson, 1982; Thelen, 1981; Thelen & Fisher, 1983). Given this trend, the importance of cardiac-somatic integration to adult attention and the relative paucity of comparable information in the infant population, there appears to be some merit in examining more closely cardiac-somatic integration and attention in the young, behaviorally alert infant. This information may have implications for understanding early neurological development (e.g., maturation of the autonomic nervous system), as well as implications for designing methodology and evaluating the merit of using both covert (e.g., heart rate) and overt (body movement) measures to infer infant attention (e.g., Miller & Byrne, 1983; Morrongiello & Clifton, 1984).

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In this regard, infants in the present study were presented photographic slides, and their visual attention, heart rate, and general body movement were monitored simultaneously. It was predicted that there would be a strong relationship between the body-movement (BdM) and heart-rate (HR) activity during visual attention, with both systems showing a deceleratory response pattern thereby facilitating attention (see Porges, 1976, 1980, for discussion). The present study was conducted as part of a series of studies in which cardiacsomatic integration is being examined in young infants. Many of the previous studies monitoring both HR and BdM have used a behavioral code to infer the degree, type, and/or direction of BdM. In the present study, BdM was recorded in digital form for each second (real time); this method of recording was thought to yield a more comparable metric to that derived for HR, thereby facilitating an analysis of cardiac-somatic integration.

METHOD Subjects Thirty-nine normal, full-term infants were tested. Data on 7 of these infants were excluded because of unstable behavioral state (crying, fussing). Of the remaining 32 infants, 11 were excluded because they failed to exhibit a minimum of 5 s of consecutive visual attention in each of the five stimulation trials. This criterion for inclusion was necessary to allow a minimum time interval for a possible change of HR in the presence of visual attention. This yielded a final sample of 21 infants (M= 14.81 weeks, SD= 1.50) on which data analyses were conducted. Procedure Each infant was fitted with electrocardiogram (EKG) electrodes and securely seated in a custom-designed infant seat. Testing was conducted inside a commercial sound-attenuated chamber. When a stable, alert behavioral state was achieved, the session was begun. The infant was exposed to a five-trial format in which a color photographic slide of a smiling female model was presented on a 25 x25 cm screen. Each stimulus (S) trial was 20 s in duration and was preceded by a no-stimulation (NS) trial that varied randomly between 20 and 27 s to reduce the possibility of a temporally conditioned response. The format was as follows: NS,/S,, NS,/S,, NSJS,, NS,/S,, NSJS,. Visual attention was monitored simultaneously for each second (real time). Stimulus presentation was controlled by a microcomputer; coincident with stimulus onset and offset, an electronic marker demarcated the trials within the session, which were recorded in the computer. Heart Rare. Infant HR was monitored by means of three EKG electrodes affixed to the chest in a modified Lead II configuration. The analog EKG signal

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was transmitted simultaneously to a Grass polygraph (Model 7D) and a microcomputer. The computer software converted the EKG analog signal to beats per minute (BPM) by calculating the duration (ms) of successive interbeat (R-R) intervals for each second (real time). Body Movement. Infant BdM was monitored by means of a custom-designed infant seat (GM Model No. 3744975). It was situated in the center of the chamber and secured on top of a 72 cm long aluminum pedestal which was supported by a 45 x 48 cm weighted, metal rectangular base. Two strain gauges were affixed to the bottom of the pedestal to detect general body movement, inferred from the peak excursion (per second) of the pedestal, within the horizontal plane. The excursion was transmitted simultaneously, as magnitude of voltage (range = O-250 mv), to the polygraph and the microcomputer; the signal was converted from analog to digital form. The signal amplitude was adjusted to accommodate the infant’s full body weight; the marker was set at point zero after the infant was seated and stationary. Visual Attention. Visual attention was monitored by two independent observers using the conventional cornea1 reflection technique; they observed through one of two small observation holes located on either side of the screen at its midsection. The observers wore headphones through which music was heard to ensure that depression of their observation key was not audible. The observation keys were interfaced with the computer and the amount of looking (ms) within each second (real time) was recorded. The minimum recorded interrater reliability was 87%.

RESULTS Data Reduction As noted earlier, only subjects who exhibited 5 s of consecutive looking during each of the five stimulation trials were included in the analyses. For each infant, HR and BdM data for the first 5 s of consecutive looking were entered into the analyses, as were the immediately preceding 5 s of no-looking. This yielded a total of ten 5-s periods-five no-look and five look periods. Heart Rate. The average HR was computed for each of the no-look and look periods. A 2 (No Look, Look) x 5 (Trials) repeated-measures ANOVA showed that there was a significant main effect of Look, F(1,20) = 22.11, p < .OOl; the infants exhibited significantly lower HR when they were attending to the stimulus (see Figure 1). There was no main or interactive effect of Trial, indicating that the magnitude of the HR deceleration did not change significantly across trials.

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Figure 1. Mean heart rate (HR) and and look (L) periods across trials.

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Body Movement. The average magnitude of BdM was computed for each of the no-look and look periods. A 2 (No Look, Look) x 5 (Trials) repeatedmeasures ANOVA also showed a significant effect of Look, F(1,20) =28.96, pc .OOl; the infants significantly decreased the magnitude of their BdM when they were attending to the target stimulus (see Figure 1). There was again no main or interactive effect of Trial, indicating the absence of a significant change in the magnitude of decreased body movement across trials. A further illustration of the relationship between the HR and BdM can be seen in the results of Pearson correlation analyses. The average HR and BdM, for each of the 5 s within the five no-look periods, were not significantly related, r(25) = .37, p > .05, but they were significantly correlated across the look periods, r(25) = .43, p-c .05. To further examine this relationship, correlation coefficients were calculated for each infant within the no-look and look periods. A t-test of related measures was conducted between the no-look and look period coefficients, and this difference did not reach significance, f(20) = 0.24,p> .05.

DISCUSSION

During visual attention, significant changes in both HR and BdM were observed; the infants exhibited both HR deceleration and decreased BdM. In addition, across the session, the magnitude of both HR and BdM were significantly correlated across periods of visual attention but not across periods of inattention. The magnitude of coefficients between these two periods did not differ significantly. This nonsignificant result may be in part due to the small sample size, but obviously future study is necessary to address this issue more fully. There are several implications of these findings. The data suggest that when presented with a target stimulus, the young infant’s autonomic system is functioning in such a way that perceptual-cognitive processes have a similar depres-

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sive or inhibitory effect on both HR and BdM. Although the exact mechanism underlying this inhibitory effect is not yet fully understood, these data suggest that there may be a system that affects not only HR but also BdM. One obvious issue is whether there exists an underlying mechanism which affects HR and BdM in a unified manner. The evidence for this in young infants is, to date, sparse and may suggest that degree of independence is age-related. Woodson and Hamilton (1986), although not examining infant attention, observed the HR and BdM of preterm newborns. In a resting state, approximately 85% of HR variance could be accounted for by general BdM, suggesting a rather high degree of interdependence in the first few days of life, at least in a resting state. In one of the few developmental studies, Morrongiello and Clifton (1984) found that newborns showed HR deceleration only with decreased motor activity (i.e., head-turning) during presentation of auditory stimuli; 5-montholds, however, exhibited HR deceleration in both the absence and the presence of motor activity, suggesting that, although HR and BdM may be highly interdependent in the newborn, maturation of central nervous system (CNS) and/or musculature may allow a more independent functioning of the HR and BdM systems. In the present study, HR and BdM were significantly related during attention but not during inattention, suggesting that by 4 months of age ongoing HR and BdM are at least sufficiently independent to yield a greater degree of synchrony during periods of attention than in periods of inattention. Although not examining directly the impact of psychological activity (attention) on HR-BdM, Woodson and Hamilton (1986) speculated that future study may show a correlation during a resting state, and psychological activity (e.g., attention) could attenuate this relationship. The present findings suggest, however, that for the older infant, at least, the psychological activity of visual attention will increase the degree of HR-BdM synchrony. It is obvious that this interpretation is preliminary. It would be interesting to examine the degree of integration during periods of attention and inattention in behaviorally alert infants throughout the first 6 months of life. It is possible that in the newborn the relatively less mature CNS may yield a high degree of cardiac-somatic integration under both conditions (attention, inattention) reflecting a “biologically imposed” interdependence. With CNS maturation, the older infant (5-6 months) may begin to exhibit a reduced level of cardiac-somatic integration in the resting period but a strong level of integration when attending to the environment. This may reflect that HR and BdM are under increasingly greater influence of higher-level cortical activity. Alternatively, increased perceptual-motor maturation may account for changes in cardiac-somatic integration (Morrongiello & Clifton, 1984; Pomerleau & Malcuit, 1980). The main objective of the present study was to determine the degree of cardiac-somatic integration during attention and inattention. In future study, utilizing the traditional habituation-dishabituation paradigm with a greater number of trials, it would be interesting to determine whether the degree of cardiac-somatic integration would decrease with repeated exposure to a visual

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stimulus; such a decrease in integration may reflect the early stages of visual habituation (i.e., looking away from target stimulus). Given the substantial differences in age of the subjects, periods of observation, measurement, and procedure, direct comparison with previous studies is difficult (e.g., Morrongiello & Clifton, 1984; Woodson & Hamilton, 1986). Nonetheless when these differences are accounted for, the interpretations of the present findings do not contradict these previous findings. Of particular interest is the cross-species similarity of these findings. Berntson and Boysen (1984) found a high degree of cardiac-somatic integration in both chimpanzees and a gorilla. Cardiac acceleration and subsequent deceleration was accompanied by similar somatic responsivity. These data attest to the possible “universality” of the cardiac-somatic relationship and, therefore, attest to its importance and need for further study. The findings of the present study also have implications for issues related to behavioral measurement and methodology. Given the young infant’s limited verbal repertoire, researchers must design paradigms and measures that encourage a response from the infant so that inferences can be made about the presence of perceptual-cognitive processing. Comparability of findings across studies and laboratories is sometimes difficult; this may be the result of different dependent measures (e.g., heart rate, body movement, visual attention) or the reliance on measures that are similar but possibly unstable. One solution is the simultaneous recording of several measures; convergence across the measures may provide stronger support for a particular finding (Morrongiello & Clifton, 1984; Stroufe & Waters, 1977). The absence of convergence across measures may allow the scientist to examine further the specific stimulus parameters yielding differential response patterns. In regard to methods of measurement, a comparative study of cardiacsomatic integration when movement is recorded with behavioral rating codes versus a digitized method seems warranted. Many studies in the past have used behavioral rating scales, employing a time-sampling procedure; behavioral codes have yielded informative data and may be the method of choice for certain behaviors (e.g., head-turning) and for lengthy periods of observation (e.g., Woodson & Hamilton, 1986). However, for recording ongoing somatic activity (e.g., BdM) the use of a digitized form of recording may yield a metric more comparable to that of HR, and thereby yield a more specific examination of their relationship. Given the phasic nature of HR deceleration to stimulus change, a system of BdM recording, such as the one employed in the present study, allows measurement across shorter periods of observation (e.g., second by second vs. 5-min time block; Woodson & Hamilton, 1986). Obviously this is an issue that warrants additional study. In summary, the results of this study suggest that integration of cardiacsomatic activity may be indicative of visual attention in the 15week-old infant. The results have implications for both CNS maturation and decisions regarding behavioral measurements upon which inferences about perceptual-cognitive processing may be made.

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REFERENCES Berg,

W.K., & Berg, K.M. (1979). Psychophysiological development: States, sensory functions, and attention. In J.D. Osofsky (Ed.), Handbook of infant development. New York: Wiley. Berntson, G.G.. & Boysen, ST. (1984). Cardiac startle and orienting responses in the great apes. Behavioral Neuroscience, 98, 9 14-9 18. Korner, A., Zeanah, C., Linden, J., Berkowitz, R., Kraemer, H., & Agras, W. (1985). Relation between neonatal and later activity and temperament. Child Developmenf, 56, 38-42. Lacey, J.I., & Lacey, B.C. (1974). Heart rate responses and behavior: A reply to Ellott. Journalof Personality and Social Psychology, 30, 1- 18. Miller, C.L., & Byrne, J.M. (1983). Psychophysiologic and behavioral response to auditory stimuli in the newborn. Infant Behavior and Development, 6. 369-389. Morrongiello, B.A., & Clifton, R.K. (1984). Effects of sound frequency on behavioral and cardiac orienting in newborns and five-month-old infants. Journal of Experimental Child Psychology, 38, 429-446. Morse, P.A., Leavitt, L.A., Miller, C.L., & Romero, R.C. (1976). Overt and covert aspects of adult speech perception. Journal of Speech and Hearing Research, 20, 154-168. Nelson, M., Clifton, R., Dowd, J., & Field, T. (1978). Cardiac responding to auditory stimuli in newborn infants: Why pacifiers should not be used when heart rate is a major dependent variable. Infant Behavior and Developmenr. I, 277-290. Obrist, P.A. (1976). The cardiovascular-behavioral interaction-as it appears today. Psychophysiology, 13. 95-107. Olson, G.M., &Sherman, J. (1983). Attention, learning, and memory in infants. In P.H. Mussen (Ed.), Handbook of child psychology: Vol2: infancy and developmental psychology. New York: Wiley. Pomerleau, A., & Malcuit, G.G. (1980). Development of cardiac and behavioral responses to a three-dimensional toy stimulation in one- to six-month-old infants. Child Development, 51, 1187-I 196. Porges, S.W. (1976). Peripheral and neurochemical parallels of psychopathology: A psychophysiological model relating autonomic imbalance in hyperactivity, psychopathology, and autism. In H. Reese (Ed.), Advances in child developmenr and behavior (Vol. 11). New York: Academic. Porges, S.W. (1980). Individual differences in attention: A possible physiological substrate. Advances in Special Education, 2, 1 I I- 134. Robertson, S.S. (1982). Intrinsic temporal patterning in the spontaneous movement of awake neonates. Child Development. 53, 1016-1021. Stroufe, L.A., & Waters, E. (1977). Heart rate as a convergent measure in clinical and developmental research. Merrill-Palmer Quarterly, 23, 3-25. Thelen, E. (1981). Rhythmical behavior in infancy: An ethological perspective. Developmenral Psychology, 17, 237-257. Thelen, E., & Fisher, D.M. (1983). From spontaneous to instrumental behavior: Kinestatic analysis of movement changes during very early learning. Child Development, 54, 129-140. Woodson, R.H., & Hamilton, C. (1986). Heart rate estimates of motor activity in preterm infants. Infant Behavior and Developmenl, 9, 283-290. 27 April

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