~ {‘1‘- CARDEAC HABETUATION T0 AR AUDITORY STIMULUS SN WELL Ax?!) MALNOURKSHED INFANTS ‘ Dissertation for the Degree of Ph. D. MECHIGAN STATE UNWERSNY BARRY MARSHALL LESTER 1973 h— LIBRARY .1 ° § _ Lichigan State *9 University l—-—- _ v- 1", -——-_ w This is to certify that the thesis entitled CARDIAC HABITUATION TO AN AUDITORY STIMULUS IN WELL AND MALNOURISHED INFANTS presented by Barry Marshall Lester has been accepted towards fulfillment of the requirements for Ph.D. degree in Psychology Date August 10 , 1973 0-7 639 : ABSTRACT CARDIAC HABITUATION TO AN AUDITORY STIMULUS IN WELL AND MALNOURISHED INFANTS BY Barry Marshall Lester This study examined the effect of nutritional insult on the magnitude and habituation of the orienting response (OR) in one-year-old male infants. Twenty well nourished and twenty malnourished infants from the lower social-economic class in Guatemala City, Guatemala, were presented with twenty trials of a pure tone stimulus. The infants were full-term, full birth weight, clinically normal and suffered no majbr illnesses during the first year of life. The design was balanced for the order of stimulus presentation. Twenty subjects were presented with ten trials of a 750 Hz tone followed by five trials of a 400 Hz tone and five trials of the 750 Hz tone. For the remaining twenty subjects this order was reversed. The tones were presented at 90 db for five seconds with a randomized inter-trial interval. The major dependent variable was heart rate deceleration and all infants were tested while in an awake and alert state. Barry Marshall Lester The results showed that for the well nourished infants each tone sequence was characterized by a large initial OR followed by rapid habituation. In contrast, there was no change in heart rate deceleration to any of the tone sequences for the malnourished infants. These infants showed an attenuation or complete absence of the OR. The results were taken as evidence of a fundamental attentional deficit associated with malnutrition that probably interferes with learning. Such a deficit, if it persists into childhood may account for the often re- ported poor performance of malnourished children on standard psychological tests. CARDIAC HABITUATION TO AN AUDITORY STIMULUS IN WELL AND MALNOURISHED INFANTS By Barry Marshall Lester A DISSERTATION Submitted to Michigan State University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY Department of Psychology 1973 To Freda who said that I could and to Hi who made sure that I did. ii ACKNOWLEDGMENTS This research was supported by Contract #PH43-65-640 from the National Institute of Child Health and Human Development and was conducted while the author was Staff Psychologist at the Institute of Nutrition for Central America and Panama (INCAP). Many thanks are expressed to a long list of people who made my two years at INCAP a rewarding and fulfilling experience. Among them are Dr. Robert Klein, Dr. Charles Yarbrough, Ms. Rosemary Metcalfe, Sra. Sonia Judith Martinez and Sr. Samuel Arevalo . and especially to Dr. Jon Berall who opened my eyes to the political and social realities of the problem of malnu- trition. I My appreciation is also extended to Drs. Ellen Strommen, Lucy Ferguson and William Crano for their par- ticipation on my Doctoral Committee and support during my graduate career. A super-special thanks goes to my Committee Chairman, Dr. Hiram Fitzgerald, who in addition to pro- viding me with support, encouragement, and guidance in my training as‘a developmental psychologist also took time out of his busy schedule to journey to the wilds of Guatemala in conjunction with this research. iii My deepest gratitude and love are expressed to my wife, Sara, and to the other members of the house, David and Cornelia Schnarch who, among other things, helped me to retain my sanity during graduate school. iv TABLE OF CONTENTS Page ACKNOWLEDGMENTS . . . . . . . . . . . . iii LIST OF TABLES . . . . . . . . ._ . . . vii LIST OF FIGURES . . . . . . . . . . . . xi INTRODUCTION 1 Infant Studies . . . . . . 1 Attention and Habituation . . . . . . . 6 Attention and Heart Rate . . . . . . . . 9 PILOT STUDY I . . . . . . . . . . . . 11 Method . . . . . . . . . . . . . 11 Results and Discussion . . . . . . . . 12 'PILOT STUDY II . . . . . . . . . . . . 15 Method . . . . . . . . . . . . . 15 Results and Discussion . .' . . . . . . 15 PILOT STUDY III . . . . . . . . .. . . . 20 Method . . . . . . . ,. . . . .. . 20 Results and Discussion . . . . . . . . 20 MAIN STUDY . . . . . . . . . . . . 23 Method . . . . . . . . . . . . . 23 Subjects . . . . . 23 Determination of Nutritional Status . . . 26 Procedure . . . . . . . . . . . . 30 Data Reduction . . . . . . . . . . 34 Results . . . . . . . . . . . . . 35 Discussion . . . . . . . . . . . . 49 Implications . . . . . . . . . . . 55 Conclusions . . . . . . . . . . . . 60 Page REFERENCES . . . . . . . . . . . . . . 64 APPENDIX . . . . . . . . . . . . . . . 72 vi Table A1. A2. A3. A4. LIST OF TABLES Analyses of Heart Rate Responses by Blocks of Five Trials for Children in Pilot StUdy I o o o o o o o o ' o 0 Age and Anthropometry of Infants in Pilot Study II . . . . . . . . . Social-economic Characteristics of Infants in Main Study . . . . . . . . Age and Anthropometry of Infants in Main Study .. . . . . . . . Experimental Design of Main Study Correlations Among Heart Rate Measures by Tone Sequence for Infants in Main Study . Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence I in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence III in Welleourished Infants by Order of Stimulus Presentation and Trials . . . . Summany of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence I in Malnourished Infants by Order of Stimulus Presentation and Trials vii Page 13 16 24 29 31 46 73 73 74 74 Table Page A5. Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 75 A6. Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 75 A7. Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I in / Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 76 A8. Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence II in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 76 A9. Summary of Analyses of Variance of Mean Heart Rate Accelration for Tone Se- quence III in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . . . . . . . 77 A10. Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 77 A11. Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 78 A12. Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence III in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 78 A13. Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 79 viii Table A14. A15. A16. A17. A18. ’A19. A20. A21. A22. A23. Page Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 79 Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III in Well Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 80 Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I in Nourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 80 Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 81 Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III in Malnourished Infants by Order of Stimulus Presentation and Trials . . . . . . . 81 Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence I by Nutritional Status and Trials . . . . . 82 Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence I (Trials 2-10) by Nutritional Status and Trials . . . . . . _. . . . . . . 82 Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence I (Trials 6-10) by Nutritional Status and Trials . . . . . . . . . . . . . 33 Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II by Nutritional Status and Trials . . . . . 83 Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II (Trials 12-15) by Nutritional Status and Trials 84 ix Table A24. A25. A26. A27. A28. A29. ' A30. A31. A32. A33. A34. A35. Summary of Analysis of Variance of Mean Heart Rate Deceleration Sequence III by Nutritional Status and Trials . . . . . . . Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence III (Trials 17-20) by Nutritional Status and Trials . . . . . . . . . . . Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I by Nutritional Status and Trials . . . Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I (Trials 6-10) by Nutritional Status and Trials . . . . . . . . . . . Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence II by Nutritional Status and Trials . Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence III by Nutritional Status and Trials Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I by Nutritional Status and Trials Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I (Trials 2—10) by Nutritional Status and Trials . . . . . . . . . Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II by Nutritional Status and Trials . . Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II (Trials 12-15) by Nutritional Status and Trials . . . . . . . . . Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III by Nutritional Status and Trials . Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III (Trials 17- 20) by Nutritional status and Trials . . . . . . . Page 85 85 86 86 87 87 88 88 89 89 90 Figure Heart for LIST OF FIGURES Rate Deceleration to Pure Tone Stimuli Infants in Pilot Study II Percent Weight for Age Distribution for 108 Lower Class Guatemalan Infants . Heart for Heart for Heart for Rate Deceleration to Pure Tone Stimuli Infants in Main Study . . . Rate Acceleration to Pure Tone Stimuli Infants in Main Study . . . . Rate Variability to Pure Tone Stimuli Infants in Main Study Percentage of Infants in Main Study who Showed the Behavioral Orientation Reactor (BOR) xi Page 18 28 39 42 44 48 INTRODUCTION Nearly two-thirds of the world's children suffer from some form of protein-calorie malnutrition (Habicht, 1972). Of recent concern is the possibility that malnu- trition may have deleterious effects on mental deve10pment, particularly when nutritional insult is suffered early in life. Several studies have demonstrated that children who were malnourished during infancy score significantly lower on tests of psychological performance than their well nour- ished counterparts (Barrera-Moncada, 1963; Cabak & Najdanvic, 1965; Monckeberg, 1968; Stoch a Smythe, 1968). For example, Stoch and Smythe (1968) compared the perform- ance of well nourished and malnourished samples on the New South African Individual Scale over an eleven year period. Sixty percent of the malnourished group fell below the level of the lowest child in the control group. Only one child in the malnourished group exceeded the mean of the control group. Infant Studies Nevertheless, few attempts have been made to di- rectly assess the effects of malnutrition on behavior during the first few years of life. Moreover, most studies which 2 have focused on infancy have been confined to reporting gross differences in psycho-motor functioning throngh the administration of infant scales. Cravioto and Robles(1965) administered the Gesell Developmental Schedules to infants hOSpitalized for malnutrition at various ages. When ad- mitted to the hospital all infants showed deve10pmental retardation. The effectiveness of nutritional rehabili- tation varied as a function of the infant’s age upon ad- mission. Infants admitted at 37-42 months of age showed significant improvement as indicated by the Gesell Devel- opmental QuotientCDQ) score. Those admitted under six months of age continued to evidence deve10pmental lag even after 6 1/2 months of hospitalization. Similarly, Chase and Martin (1970), compared the psycho—motor performance of infants who were hospitalized for malnutrition during the first year of life with a well nourished control group. No differences in performance on the Yale Developmental Scale were found between control children and those hospitalized before four months of age. However, children who were hospitalized after four months of age showed decrements in performance when compared with both the control group and those children hospitalized after four months of age. Finally, Stoch and Smythe (1963), reported DQ differences of up to twenty points between well and malnourished two year olds and other studies have also reported depressed infant scale performance among malnour- ished infants(Barrera-Moncada, 1963; Geber G Dean, 1956; 3 Monckeberg, 1968; Pollitt G Granoff, 1967). However, the age Specific effects of malnutrition are not clear since factors such as the age of onset of malnutrition (particu- larly as related to age of weaning) and the length of the disease have not been studied in relation to psychological performance. Brockman and Ricciuti (1971) used a simple sorting task to compare the cognitive development of Peruvian in- fants hospitalized for marasmatic malnutrition with a well neurished control group. The authors suggested that the poor performance of the malnourished infants reflected a retardation in the acquisition of concepts. Moreover, per- formance was lower among malnourished infants less than 24 months of age than among malnourished infants greater than 24 months. While the above studies suggest a relation between early nutritional inanition and subsequent intellectual development, there are at least two levels on which they may be criticized. First, malnutrition does not occur inde- pendent of other salient biological and social circumstances (Klein, Lester, Yarbrough, G Habicht; 1971, Birch a Gussow; 1970). Malnutrition seldom is found among the wealthy! Consequently, effects due to malnutrition per se are often confounded with other intervening factors such as social class and prenatal, perinatal and postnatal infection. These factors have been shown to interact with nutritional effects in the prediction of psychological performance, 4 (Klein, et al., 1971). Nevertheless, malnutrition is re- lated to mental deve10pment even when other environmental variables are controlled (Klein, Lester, Yarbrough, & Habicht, 1972). Another non-nutritional factor which may complicate the interpretation of previous studies is the fact that many of the malnourished children were hospitalized for varying lengths of time during nutritional rehabilitation. Thus, nutritional and institutional affects may have been confounded. A second level of criticism of the above studies relates to the use of infant deve10pmental scales as the major dependent measure of the effects of malnutrition. These scales are predominantly made up of motor test items and while they are useful as descriptors of gross psycho- motor functioning they do not adequately assess cognitive functioning. In other words, infant scales do not specify the underlying psychological processes that may be affected by malnutrition. Moreover, their power to predict later intellectual performance is often reported to be low (Bayley, 1970). Some studies have attempted to differentiate various types of performance through the further breakdown of mental and motor scores into component sub-scales, such as lan- guage or adaptive behavior. However, it is still not clear what psychological mechanisms are affected by malnutrition to produce a deficit in language performance (Chase 8 5 Martin, 1970). This same logic can be applied to the Brockman and Ricciutti study (1971): How does malnu- trition affect concept aquisition? Does an inability to discriminate among task stimuli result from a deficiency in inter-sensory organization as Brockman and Ricciutti (1971) suggest, or does some more fundamental process such as attention underlie poor discrimination performance? Clinical observation of malnourished infants has repeatedly indicated that nutritional insult interferes withfattentional processes. Indeed, apathy is one charac- teristic behavioral feature of the clinical syndrome of malnutrition (Birch 8 Gussow, 1970). The malnourished infant is universally found to be unresponsive to stimulus changes in the environment and to lack the exploratory be— havior, curiosity, and general activity so typical of the healthy infant (Correa, 1908, DeSilva, 1964; Geber 8 Dean, 1956; Stoch G Smythe, 1968). The magnitude of apathy in the malnourished infant gives meaning to the statement that "Once a child can be persuaded to smile he is well on the way to recovery" (Clark, 1951). Nevertheless, the clinical observation of atten- tional deficits in malnourished infants has not been system- atically investigated with experimental methodologies. Therefore, the purpose of the present study was to provide an experimental test of the hypothesis that the infant's ability to respond appropriately to impinging environmental stimuli is affected by nutritional insult. Attention and Habituation --Habituation refers to centrally mediated response decrement following the repeated presentation of a novel stimulus that is not accounted for by peripheral mechanisms such as receptor or effector fatigue. Habituation has become increasingly popular among infant psychologists as a tech- nique to evaluate a number of different processes such as sensory deve10pment, learning, perceptual development, attention, memory, and information processing (Jeffrey S Cohen, 1971). Habituation is related to selective attention. It enables the organism to actively ignore or filter non- salient aspects of the environment and to simultaneously increase receptivity to high priority events. If the case were otherwise, the result would be biologically disastrous since the organism would be quite at the mercy of all stimuli bombarding it at any moment without being able to discriminate biologically important from biologically un- important stimuli. The habituation paradigm is also attractive as a possible indicator of the integrity of the central nervous system (CNS) in infants suffering from nutritional insult. This hypothesis, that response decrement is related to central processes and is, therefore, relevant in the assess- ment of early cognitive development, derives from the theo- retical notions of Sokolov (1963). Sokolov suggested that 7 the organism preserves information about stimuli by forming a "neural model" of the intensity, quality, duration, and order of presentation of stimuli. This model becomes more deve10ped with each repetition of the stimulus. Each new stimulus is then compared to the model and if stimulus input coincides with its neural model, that stimulus is "recog- nized" and no orienting response (OR) occurs. However, if there is a discrepancy between an incoming stimulus and the neural model for that stimulus (if there is a mismatch between model and input) an OR is elicited. Thus, with repeated presentations of the same stimulus, a progressive response decrement is indicative of model acquisition. It follows that rate of response decrement should be related to the speed of model acquisition. If the process of habituation depends upon CNS involvement in the form of model building of prior input (Sokolov, 1963), one might expect the rate of habituation to be a sensitive measure of CNS integrity. This hypothesis receives marginal support from a study by Bronshtein, Antonova, Kamenetskaya, Luppova, and Sytova (1958) in which the habituation of sucking suppression to auditory input did not occur in about half of the infants suffering trauma at birth, whereas it did occur in three quarters of the normals. In addition, slower habituation was reported in "suspect babies" even after the signs of trauma had disappeared and the infants were judged to be clinically 8 normal. In the same study, absence of habituation to sound stimuli was reported in hydrancephalic infants. Similarly, Brackbill (1971) presented an auditory stimulus to a single anencephalic infant and found no evidence of habituation of the startle response. LaStly, Eisenberg, Coursin, and Rupp (1966) reported that whereas normal infants required from 20 to 37 trials to habituate to a change in tone, two "suspect babies" required almost twice as long, while two high-risk babies showed no evidence of habituation. Rate of habituation has also been studied in pre- mature infants. While Peiper (1963) reported habituation of a respiratory response to auditory stimuli in premature babies, Polikanina and Probatova (1965) and Polikanina (1961) reported no habituation of the OR to sound in pre- mature babies; habituation did occur in full term babies. jFinally, in a discussion of the Russian research on early insult Bronsht‘ein _e_t__a_l_. (1958) reported that premature bal>ies evidenced a delay in the rate of habituation. While the habituation paradigm has been used to discriminate norunal from "suspect babies" or premature babies, this metfliod has not been used in the assessment of infants suffering from nutritional insult. The present investigation compared orientation and habituation to an auditory stimulus in well nourished infants and in infants suffering from malnutrition. .The 9 design involved the presentation of 10 trials of a pure tone followed by 5 trials of a second tone of a different fre- quency followed by 5 trials of the original tone. The importance of this sequence of stimulus pre- sentation is that it permits a distinction between response decrement due to central mechanisms and response decrement due to peripheral mechanisms. Thompson and Spencer (1966) have/outlined nine parametric characteristics of habituation which, if met, would rule out response decrement due to peripheral mechanisms. Applying these characteristics to the present investigation would predict: (1) an OR followed by response decrement during the presentation of the first 10 trials; (2) response recovery or dishabituation to the change in tonal frequency (trials 11—15); (3) habituation of dishabituation, or response decrement to this change in tone; (4) a second dishabituation when the original tone is again presented (trials 16-20); and (5) response decrement of this second dishabituation during trials 16-20. Attention and Heart Rate Cardiac deceleration was the primary dependent variable in the present study. Cardiac deceleration as an attentional measure was first reported by the Laceys' (1959) and was viewed as the organism's way of increasing its re- ceptivity to external events. The Laceys' suggested that cardiac deceleration accompanies stimulus intake whereas cardiac acceleration is related to the startle or defensive 10 reaction. Graham and Clifton (1966) further reinforced the notion that the cardiac component of the OR is decel- eration. An alternative interpretation of cardiac deceler- ation is that a decrease in heart rate reflects a lowering of general somato-motor activity; that heart rate decreases as the organism becomes quiet (Obrist, Sutterer 8 Howard, 1969): Some support for this hypothesis was reported in a study in which cardiac decelerations to visual stimuli were accompanied by decreases in motor activity (Kagan, 1971). The clear implication is that cardiac deceleration and acceleration are manifestations of different phenomena. Whereas cardiac deceleration is viewed as an attentional response accompanied by motor quieting, cardiac acceler- Oation is indicative of behaviors that co-vary with in- creased motor activity, such as fear or boredom. Cardiac deceleration as an attentional measure has also been employed in studies involving the presentation of auditory stimuli as in the present investigation (Bridger, 1961; Horowitz, 1971). Since attentional processes were of major concern in this study, cardiac deceleration was the primary dependent measure although other indices of cardiac activity were also computed. Pilot Study I Method The purpose of the first pilot study was to deter- mine the feasibility of an experimental design in which pure tone stimuli are presented to well nourished and mal- nourished infants. The subjects were eight children ranging from 8 months to 40 months of age. Four children fully recuper- ated following severe marasmus comprised the experimental group. Four other children matched for age and sex com- prised the control group. Both experimental and control children were from the lower social-economic class (SES) of Guatemala City. The children were presented with 20 trials of a 400 Hz pure tone followed by 10 trials of a 750 Hz pure tone, followed by 15 trials of a 400 Hz pure tone. All tones were presented for five seconds at 65 db. The inter- trial interval (ITI) was randomized with a mean of 14 seconds and a range of 10 to 18 seconds. The dependent variable was heart rate calculated as a change score in cardiac activity from prestimulus to stimulus onset periods. The precise method of data reduction is described in the main study. 11 12 Results and Discussion Table 1 presents the mean heart rate decelerations, accelerations and range of heart rate by blocks of five trials for the well and malnourished groups. The magnitude of the heart rate decelerations during the 20 presentations of the first tone is of particular interest. The well nourished children showed a classic habituation pattern; the magnitude of the decelerations was substantial during the first block of trials, then gradually leveled off by the final block. In contrast, the previously malnourished children showed no such habituation pattern. Their slight heart rate decelerations remained stable across all presen- tations of the first tone. During the 10 presentations of the change in tonal frequency the well nourished group showed an increase in the magnitude of heart rate accelerations as compared to the malnourished group. These data suggested that the tonal change may have had a disquieting effect on the well nour- ished, and that in contrast to the malnourished group, the well nourished children recognized the change. These findings are also supported by the heart rate variability data. The changes in rate variability reflected substantially more heart rate activity duringthe entire experimental procedure for the well nourished than for the malnourished group. Indeed, the three heart rate measures taken together showed a general stability and lack of 13 NE emu n H «e N: cos n m « fieuzv me.¢ om.o oo.m m~.m AA.¢ oo.m ma.m oa.a m~.m oa.o om.H mw.e emammasoWHmz euz mm.m oo.m om.~ oe.m Ao.m mo.m oa.m om.m mo.e ma.~ mo.m om.m emamaesoz Ham: ~AHMHflDNflHN> OHM“ HHNfl: HHH OMGNSU Gmmz manzv oa.H om.o om.N om.~ oo.~ mm.~ mm.~ AQ.H om.H oo.H oe.~ oe.H emammwsowfimz . auz Nm.N ma.~ o~.H om.m Am.m mo.e OA.N Aw.H mm.H ow.» mm.H oa.o magmaesoz Hfimz COMHNHOHOUU< Ome HHMG: Gmmz heuzv ao.N ow.~ oa.H OA.H om.~ mH.m ms.N Hm.m om.~ oe.~ mm.~ on.m eoammasowflaz . snz om.~ mm.m om.N mw.H oo.~ ma.~ mA.N am.a mo.H om.e ma.m m¢.m emamaasoz Ham: QOH9NHOHOUOQ Guamm Hhflvm .3602 m mm mm Hm x NH «gay. x am mm mm . macaw ' l t .H sesum poflaa an :oHvHanu new mamana o>Hm mo mxuoau An momcommom ovum Hume: mo momxamn<--. H mqmJo N Or-\ A o \ :1: .2wa ‘- P WHO)" an In gag/my .<”" ‘0‘. - [\ 3 "-1 Mr Omhm . “GI-o $244344 \ ~“~"""~-. L- :c3: » 73" HCUCim / --'"“"'“‘~ 0:“: .'-. -- 3.1-12H N‘nw‘ o ”‘31.. Q‘s-0"“--.- : _ ‘~.~~-g F 1 I T T T. 1— I 00 l\ \0 Ln '3' M N F" (mdq) uoriniateoap 9191 iieaq ueew 32 34 36 38 40 24 26 28 30 20 22 8 1o 12 6 14 16 18 Trials 11 for Infants in Pilot 111111 to Pure Tone St 1011 Figure 1 .-Heart Rate Decelerat Study 11. 19 attenuated or completely absent in infants suffering from malnutrition. Furthermore, this attenuation of the OR persisted from the first presentation of a pure tone to subsequent changes in the frequency of the tone. However, because of the possible confounding effects of institution- alization and the relatively small sample size a more com- prehensive study was planned. In addition, another pre-test was planned to investigate HR recovery time. Pilot Study III @1129. The third pilot study was conducted to determine HR recovery time as it was not clear from the preceding studies whether or not the ITI was sufficiently long to allow for full HR recovery following each stimulus presen- tation. For this experiment, 5 well nourished and 5 poorly nourished one-year-old girls were presented with 10 trials of a 750 Hz pure tone at 90 db with a 30—second ITI. Results and Discussion HR recovery was calculated by dividing each 30- second ITI into six time blocks of 5 seconds each and com- paring the mean HR during each time blocks with the mean HR during the 5 seconds preceding the stimulus. For example, the mean HR during the 5 seconds preceding trial 1 was com- pared with the mean HR for the six 5 second periods following trial 1. The results showed, first, that each subject showed a fairly consistent HR recovery. The range of HR recovery time was usually within 8 seconds for any given subject across the 10 trials. Second, there were no differences in HR re- covery time between the poorly nourished and adequately 20 ’l 21 nourished groups. The mean time for HR to reach the pre- stimulus level and remain steady at that level was approxi- mately 15 seconds for both groups with a range of 7 to 22 seconds. The results of this experiment suggested that the ITI should be increased over that used in the previous ex- periments. Accordingly, it was decided to randomize the ITI with a mean of 20 seconds and a range of 15 to 25 seconds. This allowed ample time for HR recovery before the onset of the next stimulus. Furthermore, this ITI was appropriate for both well and malnourished infants as HR recovery time did not differ between these groups. However, as a result of lengthening the ITI to a mean of 20 seconds, the procedure consisting of 40 trials as in pilot study II could not be used as the experimental session would be too long. The length of the experimental session of pilot study II was approximately 15 minutes and several babies cried toward the end of the session. Given that these subjects were drawn from the same sample as those selected for the main study it was decided to limit the ex- perimental session to 10 minutes. For this reason, the design for the main study called for 20 rather than 40 trials. Two malnourished infants from the same sample were administered the 40 trial procedure as in pre-test 2 but with the lengthened ITI of mean 20 seconds. Both babies 22 cried shortly after the 20th trial (approximately 10 minutes). In addition, an analysis of HR data for these two babies showed no substantial changes in HR activity in the latter trials within each tone sequence. The final design is detailed below. Main Study Method Subjects The subjects were forty, one year old, male infants equally divided among two nutritional status groups. Subjects were recruited through State run medical clinics in Guatemala City, Guatemala. These clinics are located in the slums or "barrios" providing free prenatal, peri- natal and postnatal care for those families, all of whom are extremely poor, living in the "barrios." Mothers who brought their infants to one of these clinics for a regular 'check-up were contacted by a Guatemalan research assistant. The study was briefly explained to the mothers and those who consented to participate were asked a series of questions to assess the social-economic characteristics of the family and the medical history of the infant. Presented in Table 3 are the social-economic char- acteristics of the sample. As can be seen from Table 3, there were no differences between the well and malnourished infants with respect to the age or education of the parents or the occupation of the father. The parents were 25 to 30 years of age and received approximately four years of formal education. The fathers were mostly unskilled or semi-skilled 23 24 o o. w u m w ¢¢.N mm.m mo.N mm.m mN.N mm.v 0N.N om.¢ we.“ ou.mm uo.¢ oo.vm wosmfihsocfimz mm.m mN.Nm oo.¢ om.mm woAmfihzoz Ham: woaafixm woaafixmumfiom woaafixmcb mm M mm M League «Eu Lo defipmmsuuo mo make mo zucosvoam yogumm Macao: Hoonum mo memo» mm N mm M Monumm Henna: macho om< .AUSHm can: cw mpcwmcH mo mufiumflhouumsmau oasocououamfiuom--.m mam Hmu< Houem Hm> Hou<. Heumm am> Hou< Heuoa HHH mucoscom HH oucoSUom H oozescem oHnmflhm> macaw oucozcom each .Aesem eaez ea mpcmmcH Mom mucoscom mace kn moudmmoz epmm Hume: mcoa< mcofiumflohnoo--.o mqmmzom ecu pozocm 0:3 stum :Hmz :H mucmmcH mo ommucoUHmm--.o oustm mHmee_ om mH wH AH oH mH «H mH NH HH oH m w 5 o m e m N H .3391], \’ ‘l ml'll_lllJ _ _ u 1 n _ . 1 B _ _ _ a _ _ _ om o _ _ _ 1. _ _ _ m1 . _ _ 1 B u u u e m S _ _ . _ m. _ _ o _ n _ oe H _ . _ Homuzv m“ _ _ _ [Illa Uo£WHhsochE 9 omnz u n n " leezmcsoc :02 cm We. _ _ _ m... _ < mzoa . m mzoa . < mZOH oo 9 t J 1 1v 1 l GOu we 49 measure showed a general lack of responsivity among both groups, an inspection of the figure still shows differences in BOR magnitude and habituation between the well and mal- nourished infants. A related issue is whether or not the magnitude of HR decelerations is greater among infants who evidence a simultaneous BOR than among those who do not. A t test was calculated between the mean HR deceleration among the well nourished infants on trial 1 who showed the BOR and the mean HR deceleration on trial 1 among the well nourished infants who showed no BOR. These means were 11.54 for the BOR group (SD = 4.30) and 8.75 for the non BOR group (SD = 3.24) and were not significantly different. Discussion The results from this study reveal a clear nutri- tional effect on the infants ability to respond to and process impinging novel stimulation. The well nourished infants showed a classic habituation reaction to the re- peated presentation of a novel stimulus followed by dis- habituation and subsequent rehabituation to qualitative changes in that stimulus. The initial presentation of the tone resulted in a large OR which diminished rapidly. Re- sponse recovery, or dishabituation occurred to the two se- quences in which the frequency of the tone was changed with the intensity of the tone at a constant level. Response decrement following the two dishabituation stimuli was also 50 rapid suggesting that the habituation of the OR in the well nourished group was due to a neural inhibitory process rather than to effector or receptor fatigue. These results are similar to those reported by Lewis and Spalding (1967) in which HR decelerations averaged nine bpm to the initial presentation of an auditory stimulus and Moffitt (1968) who reported decelerations of up to twenty bpm in response to speech sounds. The decelerative responses in these two studies were obtained in six month old infants. Studies with older infants have reported similar HR changes to auditory stimuli although these studies have been criti- cized for their method of data reduction (Graham 5 Jackson, 1970). In contrast to the classic habituation response of the well nourished infants, the malnourished infants showed a general lack of responsivity.’ HR decelerations did not change following the repeated presentation of the tones. This lack of responsivity can be best described as an at- tenuation or, in some cases, a complete absence of the orienting response. HR decelerations on the initial trial of each tone sequence did not differ from those on subse- quent trials within the same tone sequence. Nor was there any evidence of dishabituation to the changes in tonal frequency. Deceleration responses to the dishabituation stimuli were not different from responses immediately pre- ceding the presentation of these stimuli. The only instance 51 in which HR decelerations were larger among the mal- nourished than among the well nourished group was during the last five trials of the first tone sequence. This was due to the fact that the well nourished infants had essentially stopped responding or habituated to the tone whereas the malnourished infants were still manifesting the same minimal level of deceleration on trials six through ten as they did on trials one through five. That the well nourished infants had habituated to the tone by thr fourth is also evidenced by the HR ac- celeration data. The only trials on which differences between the two groups were found for the acceleration response were these same trials, five through ten. Here the well nourished infants showed an increase in acceler- ations across the same trials. It seems likely, therefore, that this increase in accelerations for the well nourished infants was due to the fact that they had already habitu- ated (as evidenced by the deceleration data). The notion that HR acceleration reflects stimulus rejection and HR deceleration stimulus intake has been suggested by several investigators (e.g. Lacey,1959). The correlation results obtained from the present study further supports the notion that accelerations and de- celerations do indeed measure different processes. As shown in Table 6 the correlations between accelerations and decelerations within each tone sequence for both the 52 well and malnourished infants were in a negative direction. This also indicates that the results are not an artifact of the method of data reduction. The results from the HR variability measure are Similar to those of the deceleration data. For the well nourished infants, the initial presentation of the tone was associated with an increase in cardiac activity over the pre-stimulus level. Cardiac activity then decreased with subsequent presentations of the same tone. The dishabitu- ation stimuli produced an increase in cardiac activity which also decreased over the remaining trials. For the malnourished infants, cardiac activity did not change from pre-stimulus to stimulus onset levels following the pre- sentation of the initial tone, nor was there a change in activity when the malnourished infants were presented with the dishabituation stimuli. As was evident in Figure 5 the HR activity measure was characterized by more variability than the deceleration curve. This is because the activity measure is sensitive to both changes in acceleration and deceleration as evidenced by the positive correlations between HR activity and both decelerations and acceler4 ations (see Table 6). The results of this measure of cardiac activity can be compared with the results of studies by Porges, in which HR variability was related to attentional processes. Porges, Arnold, and Forbes (1973) found that in newborns, HR vari- 53 ability increased to tone onset and went on to suggest that magnitude of pretrial HR variability may be an index of attentional responsivity to the environment. The vari- ability measure in the Porges et_al. study was the mean HR variance calculated within a given period, such as trial onset. The present study used a change score in cardiac activity from pre-stimulus to stimulus onset periods. Therefore, the issue of resting HR variability and sub- sequent attentional responses cannot be addressed by the present data. However, both the study by Porges and the present investigation found an increase in cardiac change (variability or activity) to the onset of the tone. Thus, overall cardiac change, independent of the direction of the change, that is, deceleration or acceleration, may be a useful measure of attention. Such a measure would be particularly appropriate for research with newborns, in whom the directionality of the HR response to externalV stimulation is clearly ambigious (c.f. Graham 6 Jackson, 1970). To sum the results of the HR data, well nourished infants were found to exhibit the expected OR and habitu- ation of the OR as measured by changes in both cardiac decelerations and activity when presented with a pure tone stimulus. The same two measures also revealed response recovery or dishabituation to changes in tonal frequency. The malnourished infants, on the other hand, showed little S4 or no evidence of the OR for either measure, nor was response recovery demonstrated to the dishabituation stimuli. HR accelerations were minimal or absent among both groups of infants with the exception of the latter trials in the first tone sequence for the well nourished infants, which was perhaps a reflection of increasing boredom with the testing. The BOR measure yielded few responses among either group, although as was indicated in Figure 6 a greater per- centage of well nourished than malnourished infants did evidence the BOR. Further, the percentage of well nourished infants who showed the response declined over trials and in- creased to the two dishabituation stimuli. For the mal- nourished infants neither response decrement nor response recovery was noted. ~~ It is important to note that the mean deceleration among the well nourished infants who evidenced the BOR was not different from those in whom the response was not ob- served. This finding sheds doubt on the statement by Bridger and Reiser (1959) that a behavioral response provides an in- dependent measure of the infant's reception of the stimulus and should be used to validate cardiac responses. A more likely explanation is that the BOR is a poorer measure of central processes than is the HR response. 55 Implications The basic finding in this study, that the OR is diminished or absent in infants suffering from malnutrition provides strong evidence for a fundamental attentional deficit associated with nutritional insult. As mentioned previously, the OR is the organism's initial response to stimulation and provides the mechanism for selective at- tention. It enables the organism to detect and respond to salient aspects of the environment. OR attenuation or absence, then suggests an inability to respond to and process impinging novel stimulation. This confirms the clinical ob- servations of Birch and Gussow (1970) and others that the apathy and lack of responsivity of the malnourished infant -is due to a lack of stimulus receptivity. That magnitude of the OR is related to learning is suggested from recent studies by Zeiner and Schell (1971) and Ingram and Fitzgerald (1972). In the former study, in which a visual conditional stimulus was used, more rapid aquisition of the conditional discrimination was found among high OR magnitude adults. The Ingram and Fitzgerald inves- tigation reported similar findings in a study of classical conditioning of the skin potential response to an auditory stimulus in infants. Here conditioning was demonstrated only in high OR magnitude subjects. If magnitude of the OR does indeed predict learning, then absence or attenuation of the OR may be indicative of a learning deficit. 56 Support for this position was reported in a review of the Soviet experiments on the OR in mentally defective children (Lynn, 1967). The OR of these children to low and medium intensity stimuli was frequently absent. In an ex- periment in which a verbal instruction was preceded by a neutral stimulus, normal children produced an OR to the neutral stimulus and were conditioned to it whereas men- tally defective children showed neither the OR, nor evi- dence of subsequent conditioning. These results were taken as an indication of deficits in cortical functioning. The role of the cortex in orienting was also eval- uated in the Brackbill (1971) study in which an anenceé phalic infant evidenced a strong OR that did not habituate. Her conclusion was that "the cortex may not be important to the elicitation of a response, but it is essential to in— hibition of response" (1971, p. 12). While these results may appear contrary to the Soviet investigations both can be explained according to the model proposed by Sokolov (1963). According to this model the OR can occur either through direct stimulation of the recticular activating system (RAS) or as mediated by the cortex. This also permits comparison of the performance of the malnourished infants in the present study with that of the mentally defective children reported in the Soviet literature. Absence of the OR in both groups may be due to lack of communication between the cortex and the RAS 57 or to a deficit in the RAS or cortex itself. Although the explanation of the absence of the OR remains obscure the implication that OR absence or attenuation retards learning seems warranted. This suggests that the kind of deficits found in the present study, if they persist into childhood, can account, at least partially, for the often reported poor performance of malnourished children on standard psychological tests. Obviously, whether or not the effects of malnu- trition are reversible cannot be determined from the present study. Research with animals has shown that malnutrition can lead to structural damage to the central nervous system (Dobbing, 1970; Lester, 1970). Moreover, there is mounting evidence to suggest that the consequences of malnutrition are most severe for the developing brain. For example, in one study,-reduction of adult rat body weight by 40 to 50 percent failed to produce a reduction in brain weight (Peters E Boyd, 1966). The chemical composition of the brain as measured by both RNA and DNA concentrations was also found to be unaffected by similar reductions in body weight (Lehr 8 Gayet, 1963). On the other hand, when rats were malnourished during the period of rapid brain growth, which occurs entirely postnatally during the first twenty one days, severe and permanent effects were reported. Deficits in brain weight were found by Dobbing (1968) and Benton, Moser, Dodge, 8 Carr (1966). The latter study also 58 reported a reduction in total brain lipids, phospholipids, and cholesterol. Winick and Noble (1966) found a reduction in the rate of cell division and in the total number of brain cells. Other studies on the develOping rat brain have related malnutrition to deficits in protein synthesis (Zamenoff, Marthens, & Margolis, 1968), a reduction in protein content (Chase, Lindsley, & O'Brien, 1969) and incomplete myelination (Chase, Dorsey, & McKhann, 1967). Finally, studies on the deve10ping pig brain have yielded similar CNS damage as a result of malnutrition (Stewart 6 Platt, 1968; Dobbing, 1968). Dobbing (1970) has taken this evidence to suggest a vulnerable periods hypothesis which states that in any species brain development may be most susceptible to damage if insult occurs during the period of rapid brain growth. In terms of such an hypothesis, the human brain would be most sensitive to nutritional insult from the last trimester of pregnancy through the first few years of life. There is some support from human studies for the idea that the effect of nutritional insult on intelligence is most severe when insult is suffered early in life. Studies by Chase and Martin (1970), Cravioto and Robles (1965), and Stoch and Smythe (1963) which were reviewed earlier found that performance on an infant scale was lower in infants who suffered malnutrition during infancy 59 than among infants for whom insult occurred later in life. For example, in the report by Cravioto and Robles (1970), DQ performance recovered among infants hospitalized between 37 to 42 months of age whereas infants who were hospitalized prior to six months showed no recovery in DQ during com- parable periods of hospitalization. While the interpretation of the data from these studies remains equivocal due to in- adequate controls for confounding variables such as social class, hospitalization, and parental education, they do suggest that the infancy period may be one of particular susceptibility to the long term consequences of nutritional insult, It is also interesting to note that the kind of learning deficit suggested by the results of the present study, that of a deficiency in attentional process, has also been associated with low birth weight infants (Caputo 6 Mandell, 1970). While studies of low birth weight infants suffer from some of the same problems as do studies of mal- nourished infants, that is, confounding effects of social class and the exclusive use of infant deve10pmental scales, there is a striking similarity between the effects of low birth weight and malnutrition. Several authors have sug- gested that the consequences of low birth weight include disturbances in brain functioning (Caputo & Mandell, 1970; Wiener, 1965). Moreover, there is also evidence to suggest that attentional processes are affected by low birth weight. 60 For example, Drillen (1961) as well as Pasamanick (1965) found lack of concentration to be.one of the major handi- caps of school aged children born of low birth weight. I Finally, several studies have shown that reading is one of the primary abilities to be affected by low birth weight (DeHirsch, Jansky, G Langford, 1964; Rabinovitch, Bibace, 8 Caplan, 1961). These authors have interpreted their findings as reflecting a deficit in the infant's ability to receive information from the environment. These findings lend further support to the notion that early insult in general may have long term consequences for intellectual deve10pment and specifically that a direct result of early insult may be a deficit in attentional processes. Conclusions There are two main conclusions to be drawn from this study. First, infantile malnutrition affects the infant's basic ability to r95pond to and process impinging novel stimulation. The absence or attenuation of the OR reflects an attentional deficiency that probably has serious consequences for subsequent learning. Thus, there is the image of the malnourished infant as "out of touch" or un- responsive to his environment. It seems extremely likely that such an attentional handicap may impair learning and be responsible for the often reported poor performance of malnourished children on standard psychological tasks. 61 Obviously, the kind of research called for is to examine the long term consequences of this deficiency. 'Longitudinal studies which follow malnourished infants through school age are most appropriate. ‘Simultaneously, the question of the reversibility of the effects of mal- nutrition could be approached through studies in which intervention is an experimental treatment at both younger and older ages. Another approach is to expand the design of the present study to further elaborate the nature of this at- tentional deficit. The issue of sex differences, for example, was not addressed in the present investigation. It would also be useful to determine to what extent the effect demonstrated in this study was a function of the modality tested. Studies exploring the habituation of the OR with visual stimuli, for example, would contribute to our understanding of the generality of the deficit. With older children, the Zeaman and House (1963) model might prove fruitful in the investigation of the. relation between attention and nutritional insult. This theory assumes that discrimination learning requires the acquisition of two responses, an attentional response which precedes an instrumental response. By plotting learning curves these authors found that while rate of learning, once it starts, is generally independent of the number of trials, the number of trials for learning to start varies 62 considerably. It is this early portion of the curve, the number of trials for learning to start, that is presumed to be controlled by attentional processes; in- strumental processes take over once learning has begun. If attentional processes are affected by malnutrition one might predict that the number of trials for learning to start is related to the nutritional status of the child. Likewise, rate of learning, once it starts, should be relatively unaffected by nutritional insult. Finally, one would like to examine the effect of nutritional insult on other behaviors. Are all learning situations similarly affected? If magnitude of the OR is indicative of learning, then conditionability should be affected by malnutrition both in terms of the rate of aquisition of a conditioned response and as related to OR magnitude. It might also be interesting to examine the extent to which this deficit can be overcome in the face of nutritive reinforcement. The procedures employed by Papousek (1968) are appropriate as they involve the elaboration of conditioned head turning with food as reinforcement. The second major conclusion from this study is a methodological one. This is simply that the habituation paradigm was effective in uncovering differences due to malnutrition. This technique could readily be applied to other infant risk p0pu1ations, such as low birth 63 weight infants and has the advantage of measuring specific cognitive processes as Opposed to the DO approach. The use of psychophysiological measures should also be under- scored as sensitive indicators of possible dysfunction. Had the present study relied solely on behavioral measures the dramatic differences between well and malnourished infants would probably have been obscured. The importance of these findings can hardly be exaggerated. The probability that two thirds of the world's children may be suffering from intellectual im- pairment as a result of poor feeding is staggering! That governments are aware of the problem and have chosen to do nothing about it is disgraceful! How is it possible that there are over ten million Americans living on diets having less than two thirds of the minimum nutrients _ required for adequate health (U.S. Senate Select Committee on Nutrition and Human Needs, 1969)? Nutritional re- habilitation programs must include psychological as well as physical intervention as we are well aware of the potentially devastating effects of stimulus deprivation often associated with institutional care. It is only through such programs that we can help the suffering infant relearn to interact with his environment. In so- called developing countries, such as Guatemala, the infant is particularly vulnerable as early weaning on protein deficient diets often leads to nutritional inanition within the first year of life. REFERENCES 64 REFERENCES Barrera-Moncada, G. Estudios sobre alteraciones del crecimiento y del dessarrollo psicologico del sindrome pluricarencial (Kwashiorkor), Editora Grafos, Caracas, Venezuela, 1963.‘ Bayley, N. 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Government Printing Office, 1969. Wiener, G. Psychologic correlates of premature birth: A review. Journal of Nervous and Mental Disease, 1962, 134, 129-144. ' ' Winick, M., 5 Noble, A. Cellular response of rat during malnutrition at various ages. Journal of Nutrition, 1966, 33, 3-12. Zamenof, S., van Marthens, E., G Margolis, F. DNA (cell number) and protein in neonatal brain: Alteration by maternal dietary protein restriction. Science, 1968, 1323 322-332. 71 Zeaman, D., 6 House, B. J. The role of attention in retardate discrimination learning. In N. R. Ellis (Ed.), Handbook of Mental Deficienc , New York: McGraw-HiII, 1963. Pp. 158-223. Zeiner, A. R., G Schell, A. M. Individual differences in orienting conditionability, and skin resistence responsivity. Psychophysiolggy, 1971, 3, 612-622. APPENDIX 72 73 APPENDIX TABLE l.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence I in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 71.12 1 71.12 3.22 Error 353.44 16 22.09' Trials 1246.42 9 138.49 8.82 .001 Trials X Order 131.22 9 14.58 .93 Error 2261.16 144 15.70 Total 4063.37 179 APPENDIX TABLE 2.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence II in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 6.94 l 6.94 .70 Error 158.98 16 9.94 Trials 628.00 4 157.00 12.35 .001 Trials X Order 37.11 4 9.28 .73 Error 813.69 64 12.71 Total 1644.72 89 74 APPENDIX TABLE 3.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence III in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 0.00 l 0.00 0.00 Error 369.60 15 24.64' Trials 385.32 4 96.33 6.6 .001 Trials X Order 98.17 4 24.54 1.68 Error 867.29 60 14.45 Total 1720.38 84 APPENDIX TABLE 4.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence I in Malnourished Infants by Order of Stimulus Presentation and Trials. Source 58 df MS F P Order 2.65 l 2.65 .11 Error 420.61 18 23.37 Trials 115.51 9 12.83 .69 Trials X Order 233.91 9 25.99 1.41 Error 2995.89 162 18.49 Total 3768.56 199 75 APPENDIX TABLE 5.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence II in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 5.71 l 5.71 .17 Error 516.29 15 34.42' Trials 24.87 4 6.22 .30 Trials X Order 94.38 4 23.60 1.13 Error 1256.56 60 20.94 Total 1897.82 84 APPENDIX TABLE 6.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 46.94 1 46.94 1.82 Error 412.18 16 25.76 Trials 101.27 4 25.32 1.68 Trials X Order 49.44 4 12.36 .82 Error 966.49 64 15.10 Total 1576.32 89 76 APPENDIX TABLE 7.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Se- quence I in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 6.08 l 6.08 .25 Error 392.56 16 24.54' Trials 219.47 9 24.39 2.36 .025 Trials X Order 48.35 9 5.37 .52 Error 1486.89 144 10.33 Total 2153.35 179 APPENDIX TABLE 8.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Se- quence II in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 3.21 l 3.21 .39 Error 131.29 16 8.21 Trials 57.04 4 14.26 1.25 Trials X Order 26.96 4 6.74 .59 Error 731.60 64 11.43 Total 950.10 89 77 APPENDIX TABLE 9.--Summary of Analyses of Variance of Mean Heart Rate Acceleration for Tone Sequence III in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 22.61 1 22.61 2.59 Error 130.80 15 8.72' Trials 18.93 4 4.73 .43 Trials X Order 29.05 4 7.26 .66 Error 655.89 60 10.93 Total 857.28 84 APPENDIX TABLE 10.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Se- quence I in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order .02 1 .02 .00 Error 107.70 18 5.98 Trials 46.22 9 5.14 .73 Trials X Order 65.08 9 7.23 1.03 Error 1133.70 162 6.70 Total 1352.72 199 78 APPENDIX TABLE ll.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Se- quence II in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 22.49 1 22.49 1.64 Error 205.59 15 13.67 Trials 38.99 4 9.75 1.18 Trials X Order 35.60 4 8.90 1.08 Error 496.71 60 8.28 Total 798.87 84 APPENDIX TABLE 12.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Se- quence III in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F P Order 1.34 l 1.34 .30 Error 71.11 16 4.44 Trials 88.16 4 22.04 2.45 Trials X Order 64.38 4 16.09 1.79 Error 576.67 64 9.01 Total 801.66 89 79 APPENDIX TABLE 13.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Se- quence I in Well Nourished Infants by‘ Order of Stimulus Presentation and Trials. Source . . SS». df MS F ,P Order 12.72 1 12.72 .30 Error 678.64 16 42.42 Trials 657.37 9 73.04 3.02 .005 Trials X Order 404.39 9 44.93 1.24 Error 5202.86 144 36.13 Total 6955.98 179 APPENDIX TABLE l4.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Se- quence II in Well Nourished Infants by Order of Stimulus Presentation in Trials. Source SS df MS F P Order 20.54 1 20.54 1.15 Error 286.72 16 17.92 Trials 809.11 4 202.28 12.96 .001 Trials X Order 103.07 4 25.77 1.65 Error 998.62 64 15.60 Total 2218.06 89 80 APPENDIX TABLE 15.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Se- quence III in Well Nourished Infants by Order of Stimulus Presentation and Trials. Source SS df MS F .P Order 1.32 1 1.32 .04 Error 533.10 15 35.54 Trials 501.26 4 125.31 5.80 .001 Trials X Order 58.53 4 14.63 .68 Error 1295.87 60 21.58 Total 2390.08 84 APPENDIX TABLE 16.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Se- quence I in Malnourished Infants by Order of Stimulus Presentation and Trials. df MS Source SS F P Order .01 1 .01 00 Error 972.89 18 54.05 Trials 377.85 9 41.98 1.42 Trials X Order 326.05 9 36.23 1.23 Error 4790.41 162 29.57 Total 6467.20 199 81 APPENDIX TABLE 17.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II in Malnourished Infants by Order of Stimulus Presentation and Trials. Source SS df .MS 4 F .P Order .51 1 .51 .01 Error 733.51 15 48.90 Trials 32.25 4 8.06 .33 Trials X Order 154.65 4 38.66 1.60 Error 1451.21 60 Total 2372.13 84 APPENDIX TABLE 18.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III in Malnourished Infants by Order of Stimulus Presentation and Trials. Source 88 df MS F P Order 31.21 1 31.21 1.21 Error 414.09 16 25.88 Trials 240.62 4 460.16‘ 1.54 Trials X Order 62.84 4 15.71 .40 Error 2502.13 64 39.40 Total 3250.90 89 ii‘t “ELI“ 82 APPENDIX TABLE 19.--Summary of Analysis of Variance of Mean Heart Deceleration for Tone Sequence I by Nutritional Status and Trials. Source SS df MS F P Nutrition .17 1 .17 .01 Error 847.82 36 23.55 Trials 533.93 9 59.33 3.42 .001 Trials X Nutrition 875.62 9 97.29 5.61 .001 Error 5622.18 324 17.35 Total 7879.72 379 APPENDIX TABLE 20.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence I (Trials 2-10) by Nutritional Status and Trials. Source SS df MS F P Nutrition 67.46 1 67.46 2.66 Error 913.71 36,” 25.38 Trials 152.38 8 19.05 1.06 Trials X Nutrition 134.55 8 16.82 .94 Error 5162.98 288 17.93 Total 6431.09 341 83 APPENDIX TABLE 21.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence I (Trials 6-10) by Nutritional Status and Trials. Source SS df MS F P Nutrition 106.41 1 106.41 5.36 .05 Error 733.99 37 19.84 Trials 11.92 4 2.98 .18 Trials X Nutrition 7.84 4 1.96 .12 Error 2458.27 148 16.61 Total 3318.44 194 APPENDIX TABLE 22.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence II by Nutritional Status and Trials. MS Source SS df F P Nutrition 57.25 1 57.25 2.75 Error 687.92 33 .20.85 Trials 265.31 4 66.33‘ 3.98 .001 Trials X Nutrition 368.05 4 92.01 5.52 .001 Error 2201.74 132 17.51 Total 3580.28 174 84 APPENDIX TABLE 23.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II (Trials 12-15) by Nutri- tional Status and Trials. Source SS df MS F P Nutrition 10.01 1 10.01 .59 Error 607.45 36 16.87 Trials 45.39 3 15.13 .84 Trials X Nutrition 24.91 ' 3 8.30 .46 Error 1940.45 108 17.97 Total 2628.20 151 APPENDIX TABLE 24.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Sequence II by Nutritional Status and Trials. Source SS df MS F P Nutrition .13 l .13 .01 Error 828.72 33 25.11 Trials 199.37 4 49.84 I 3.32 .025 Trials X “'j Nutrition 287.12 4 71.78 4.78 .001 Error 1981.39 132 15.01 Total 3296.75 174 85 APPENDIX TABLE 25.--Summary of Analysis of Variance of Mean Heart Rate Deceleration for Tone Se- quence III (Trials 17-20) by Nutritional Status and Trials. Source .85 df MS . F P Nutrition 34.11 1 34.11 1.42 Error 840.13 35 24.00 Trials 95.84 3 31.95 1.86 Trials X Nutrition 39.51 3 13.70 .77 Error 1806.79 105 17.21 Total 2816.38 147 APPENDIX TABLE 26.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I by Nutritional Status and Trials. Source SS df MS F P Nutrition 20.44 1 20.44 1.45 Error 506.36 36 14.07 Trials 109.46 9 12.16 ' 1.44 Trials X Y ' -. Nutrition 165.65 ' 9 18.41 2.19 .025 Error 2734.02 324 8.44 Total 3535.93 379 86 APPENDIX TABLE 27.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence I (Trials 6-10) by Nutritional Status and Trials. Source SS df MS F P Nutrition 74.97 1 74.97 4.19 .05 Error 661.90 37 17.89 Trials 13.52 4 3.38 .36 Trials X Nutrition 81.19 4 20.30 2.17 Error 1381.88 148 9.34 Total 2213.47 194 APPENDIX TABLE 28.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence II by Nutritional Status and Trials. ‘ Source 58 df MS F P Nutrition 2.30 1 2.30 .21 Error 362.08 33 10.97 Trials 64.05 4 16.01 1.64 Trials X Nutrition 28.08 4 7.02 .72 Error 1290.86 132 9.78 Total 1747.37 174 87 APPENDIX TABLE 29.--Summary of Analysis of Variance of Mean Heart Rate Acceleration for Tone Sequence III by Nutritional Status and Trials. Source SS df MS F‘ P Nutrition .04 1 .04 .01 Error 225.87 33 6.84 Trials 73.12 4 18.28 1.82 Trials X Nutrition 31.71 4 7.93 .79 Error 1325.99 132 10.05 Total 1656.72 174 APPENDIX TABLE 30.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I by Nutritional Status and Trials. Source 88 df MS F P Nutrition 57.23 1 57.23 1.24 Error 1664.30 36 46.23 Trials 675.67 9 75.07 2.27 .025 Trials X Nutrition 418.55 9 46.51 1.41 Error 10723.70 324 . 33.10 Total 13539.45 379 88 APPENDIX TABLE 31.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence I (Trials 2-10) by Nutri- tional Status and Trials. Source SS df MS F P Nutrition 9.97 l 9.97 .24 Error 1505.23 36 41.81 Trials 388.05 8 48.51 1.40 Trials X Nutrition 257.03 8 32.13 .92 Error 10010.57 288 34.76 Total 12170.85 341 APPENDIX TABLE 32.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II by Nutritional Status and Trials. Source SS df MS F P Nutrition 58.84 1 58.84 1.86 Error 1041.31 33 31.55 Trials 454.68 4 "113.67 5.54 .001 Trials X Nutrition 361.08 4 90.27 4.40 .001 Error 2707.53 132 20.51 Total 4623.43 174 89 APPENDIX TABLE 33.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence II (Trials 12-15) by Nutri- tional Status and Trials. Source SS df MS F P Nutrition 8.53 1 8.53 .26 Error 1202.47 36 33.40 Trials 18.82 3 6.27 .30 Trials X Nutrition 20.74 3 6.91 .33 Error 2249.43 108 20.83 Total 3499.98 151 APPENDIX TABLE 34.--Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III by Nutritional Status and Trials. Source SS df MS F P Nutrition 4.36 1 4.36 .15 Error ‘ 979.75 33 29.69 Trials 125.42 4 31.36 1.06 Trials X Nutrition 622.20 4 155.55 5.24 .001 Error 3919.36 132 29.69 Total 5651.09 174 90 APPENDIX TABLE 35.-- Summary of Analysis of Variance of Mean Heart Rate Variability for Tone Sequence III (Trials 17-20) by Nutri- tional Status and Trials. Source 58 df MS F P Nutrition 84.74 1 84.74 ‘ 3.26 Error 909.76 35 25.99 Trials 71.97 3 23.99 .80 Trials X Nutrition 138.51 3 46.17 1.54 Error 3154.89 105 30.05 Total 4359.87 147 ‘JI‘IIIII. "I11111111171111111111“