Ethological Approach to Autism Spectrum Disorders

Abstract

The purpose of the study was to develop a new ethogram for the assessment of children and adolescents with autism spectrum disorders (ASD) and intellectual developmental disorder (IDD) and to test whether this instrument accurately distinguishes ASD participants (n = 61) from IDD participants (n = 61). An ethogram with 88 behavior elements was generated, including body postures, verbalizations, facial expressions, motor stereotypies, head postures, gaze behavior, gestures, and interpersonal distance. Significant differences were detected between both groups in classic ASD behaviors; in behaviors that are deficient in ASD according to established theoretical models, such as symbolic play, gaze direction, gaze following, and use of mental state language; in atypical behaviors that have also been described previously in ethological studies with ASD; and in the nonspecific behaviors of ASD, such as walk, look own body, explore, and cry. The predictive success of a diagnosis of ASD in the logistic regression model with the ethogram's factors was 98.4%. The results suggest that this ethogram is a powerful and useful tool for both the detailed study of the social behaviors of autistic children and adolescents, and for discriminating ASD and IDD.

Keywords

autism intellectual disability children social behavior ethology

Introduction

Modern ethology - that is, the science specialized in the evolutionary study of animal behavior - was founded by Lorenz, Tinbergen, and von Frisch (e.g., Lorenz, 1974; Tinbergen 1974). It was subsequently expanded and elaborated with regard to human behavior by Eibl-Eibesfeldt (1989). In this paper, we aim to show how the methodology of ethologists can be successfully employed to autism spectrum disorders. Autism spectrum disorders (ASD) are characterized by marked deficits in social reciprocity, social use of communication, and by the presence of repetitive and stereotyped behaviors or interests (American Psychiatry Association, 2013). The diagnosis of ASD is based on direct behavioral observation or on information about patterns of behavior and symptoms described by caregivers (Huerta and Lord, 2012). Often, the distinction between ASD and other developmental disorders, such as Intellectual Developmental Disorder (IDD), seems vague and ill-defined (Nazeer and Ghaziuddin, 2012). As children with ASD frequently have severe verbal communication deficits, the powerful and non-invasive observation methods of ethology may contribute significantly to the development of a more accurate and valid strategy for measuring the behavior of children with ASD (Klein, 2000).

A starting point in many ethological studies is the compilation of a detailed ethogram, which is a thorough descriptive catalog of the behavior patterns that form the basic behavioral repertoire of the study subjects (Troisi, 1999). Observed behaviors may differ in duration. Brief behaviors are called point-events (e.g., show, point, sit down). Lasting-events are behaviors of longer, but varying, duration (e.g., current status, interpersonal distance) (van Engeland, Bodnàr, and Bolhuis, 1985).

Autism spectrum disorders have drawn the attention both of ethologists and evolutionary psychologists due to their complexity and severe impact on the social life of affected individuals (e.g., Baron-Cohen, 2009; Reser, 2011; Tinbergen and Tinbergen, 1972; Zabel and Zabel, 1982). Elisabeth Tinbergen and Niko Tinbergen, for example, formulated a theory of the etiology of ASD couched in ethological terms (Tinbergen and Tinbergen, 1972), but the absence of evidence for their claims and the lack of precision with which they used the terms “autism” and “Kanner's syndrome” prevented their theory from having subsequent influence (Wing and Ricks, 1976). Ethological studies of ASD have focused on: systematic behavioral observations, i.e., recordings of preselected, well-defined behaviors cataloged on a timed sampling schedule; quantitative measurements of the frequencies of point events or relative durations of the behaviors (e.g., lasting-event categories); and detailed descriptions of behavior (Castell, 1970; Churchill and Bryson, 1972; Hutt and Ounsted, 1970; O'Connor and Hermelin, 1967; Pedersen and Schelde, 1997; Richer and Coss, 1976; Richer and Richards, 1975; van Engeland et al., 1985). Nevertheless, in the majority of these studies, the sample was relatively small and/or there were no comparison groups with other mental disorders, weakening their validity and specificity. Therefore, the aims of this study were to develop a new, detailed, valid, and useful ethogram with a large sample of children and adolescents with ASD, according to DSM-5 criteria, and to test whether this instrument accurately distinguishes ASD from IDD, another developmental disorder that is usually diagnosed in childhood.

Materials and Methods

Participants

All of the children and adolescents with ASD and IDD enrolled in this study were patients of the Child and Adolescent Psychiatry outpatient clinics of the Hospital of the University of Campinas (Unicamp) located in Campinas, São Paulo, Brazil. The initial sample consisted of 146 participants (69 with ASD and 77 with IDD) between the ages of 3 and 18 years (M = 10.8, SD = 4.1). The sample was composed predominantly of males (n = 113; 77.4%) and of children (n = 76; 52.1%). Clinical psychiatrists with an average of 20 years of experience treating patients diagnosed the participants using DSM-IV-TR (American Psychiatric Association, 2000) criteria for ASD and IDD. Both groups also met the proposed revised diagnostic criteria for ASD and IDD in the DSM-5 (American Psychiatric Association, 2013). The ASD participants comprised 69 children and adolescents diagnosed with ASD between the ages of 3 and 18 years (M = 9.4, SD = 4.6). The 77 IDD participants were children and adolescents between the ages of 4 and 16 years (M = 12.0, SD = 3.1). Sixty-seven participants were receiving psychotropic medication, among which antipsychotics and serotonin reuptake inhibitors were the most frequently prescribed substances.

After the participants' entry into the study, the diagnosis of ASD was confirmed by the Brazilian version of the Childhood Autism Rating Scale (CARS-BR; Pereira, Riesgo, and Wagner, 2008), which is a behaviorally-based rating scale used to evaluate the severity of autistic symptoms. Also following their entrance into the study, all participants with IDD between the ages of 6 and 16 years completed the Wechsler Intelligence Scale for Children or Adults, 3rd edition, Brazilian version (Wechsler, 2002, 2004), to determine their full-scale IQ (FSIQ). Participants with IDD aged less than 6 years were intellectually assessed with the Columbia Mental Maturity Scale (CMMS; Burgemeister, Blum, and Lorge, 2011). The two groups were matched in chronological age. Table 1 presents the results of the comparison between the ASD and IDD groups regarding age, gender, and CARS-BR total score.

Table 1.

Sample characteristics (n = 122)

	ASD (n = 61)		IDD (n = 61)		p-value

Continuous Variables	Mean	SD	Mean	SD
Age	9.5	4.7	10.8	2.2	0.109
CARS-BR	41.6	7.7	17.6	5.9	< 0.001

Categorical Variables	n	%	n	%

Gender
Male	55	90.1	49	80.3	0.126
Female	6	9.9	12	19.7

Age Group
Children	37	60.6	38	62.2	0.852
Adolescent	24	39.4	23	37.8

Notes: ASD = Autism Spectrum Disorders; IDD = Intellectual Developmental Disorder; Significant values in bold

A group of 24 participants (16.4%) was excluded from the main analyses as they could not be unequivocally categorized as either ASD or IDD, according to the CARS-BR cutoff score (< 30) for ASD and the WISC-III/ WAIS-III or CMMS cutoff score for IDD (IQ < 70 or Age Deviation Score below two standard deviations in CMMS). This group was analyzed separately, in order to verify if these individuals could also be categorized based on the ethogram. Parents signed consent forms approved by the Institutional Review Board of Unicamp.

Measures

Video recorder. A high-definition hidden camera pen (by Brickhouse) with a digital video recorder (1280 × 720 pixels, 30 frames per second, 8 gigabytes), audio video interleaved format (AVI), and high speed universal serial bus (USB) 2.0 interface was used to record each participant during their regular psychiatric assessment.

Ethogram. We developed an ethogram from observations of the study participants' social behaviors in outpatient clinics of the Unicamp Hospital. This ethogram also incorporates measures from the literature of social behaviors of children with ASD in naturalistic settings, such as gaze and physical aversion, interpersonal distance, joint attention, mental state language, and other communication skills (Chiang, 2008, 2009; Hutt and Ounsted, 1970; Jones and Schwartz, 2009; Macintosh and Dissanayake, 2006; Perdersen and Schelde, 1997; Richer and Coss, 1976; van Engeland et al., 1985). To compose the categories and subcategories of the ethogram, we selected the first 10 recordings from ASD and IDD participants, for a total of 20 recordings. The All Occurrences Sampling method was used to analyze the video recordings. In this method, all behaviors observed within a period of time are included in the ethogram (Altmann, 1974; Setz, 1991). The final categories of the ethogram included body postures, verbalizations, motor stereotypies, head postures, gaze behavior, gestures, current status, and interpersonal distance (see Appendix I). Additionally, we developed two scoring sheets to facilitate the count of point- and lasting-event categories during the video recording analyses (see Appendices II and III).

Procedure

All the participants were videotaped in the outpatient clinics of the Unicamp Hospital during a follow-up psychiatric assessment in the company of their mothers, in a 343 cm × 230 cm room containing one table, four chairs, one gurney, one trash can, and one sink. Video recordings of each patient generally lasted 15 minutes, and the participants were inside the room for the duration of the recording. The parents knew about the recording, but the patients did not. The first author of the present study operated the video recorder pen but avoided interaction with the participants, caregivers, and psychiatrist.

Video recordings of each participant were analyzed using the All Occurrences Sampling method (Altmann, 1974; Setz, 1991), with a time interval of 2 minutes for point-events (e.g., point, look, talk), resulting in five periods of continuous analysis (i.e., measurements at 0–1, 3–4, 6–7, 9–10, and 12–13 minutes; see Appendix II), as well as the Scan Sampling method (Altmann, 1974; Setz, 1991), with intervals of 1 minute for lasting-event categories, totaling 15 distinct instantaneous scans (see Appendix III). In the Scan Sampling method, one records the lasting-event categories (e.g., an individual's current activity or interpersonal distance) at preselected moments in time. The first author of the present study analyzed the video recordings and was not blind to the diagnosis of the participants during the video recording and the coding process.

Statistical analysis

The data were analyzed using the Statistical Package for the Social Sciences (SPSS) version 17.0. The variables were tested for normality using the Kolmogorov-Smirnov test. An arcsine square root transformation (ASRT) for lasting-event categories was performed. The ARST has long been a standard procedure when analyzing proportional data in ethology (Sokal and Rohlf, 1995; Zar, 1998). The frequency of each behavior element (i.e., the subcategories of our ethogram) was computed for each participant, and the frequencies in the experimental group (ASD) were compared with those in the control group (IDD). Mann-Whitney's test was used to compare age and the frequencies of behavioral elements between participants with ASD and IDD. A Chi-square test was used for the comparison of gender.

In order to reduce the subcategories of the ethogram to a small set of variables, a principal components factor analysis (eigenvalues ≥ 1) with Varimax rotation and Kaiser Normalization was performed on the total sample. The subcategories of the ethogram were standardized for the analysis due to differences in the variables. Factors with eigenvalues larger than 1 were initially extracted using principal components. The scree plot was then examined using Cattell's (1966) point of inflection criterion to determine factor numbers. Only behavior elements with a factor value in excess of 0.40 were used in this analysis, and elements that loaded on two different factors with a difference of factor loadings less than 0.20 were eliminated. The reliability analysis was performed on the final ethogram to assess the internal consistency as measured by Cronbach's alpha.

Two binary multivariate logistic regression analyses, with backward likelihood ratio selection method, were conducted with the ethogram's new factors and with 10 main ethogram categories (i.e., the sum of the frequencies of each subcategory) to explore the predictors of the ASD diagnosis.

Results

We collected 2,190 minutes (36.5 hours) of video recordings for the total sample. The full analysis of the 2,190 minutes of recording took 13,140 minutes, or 219 hours - 90 minutes per participant. The final ethogram comprised 10 major categories divided into 88 subcategories, 67 of which described point-events, and 21 of which described lasting-event categories (see Appendix I for an overview of the main categories, their behavioral elements, and a brief description of each element). Of the 88 subcategories in the ethogram, participants with ASD and IDD showed significant differences in 77 subcategories. Eleven subcategories did not differentiate between ASD and IDD (see Table 2). This could be related to the large variation within the samples, and not necessarily a lack of difference between ASD and IDD. Children and adolescents that were excluded from the main analyses, based on difficulties in categorizing them according to standard diagnostic checklists for ASD and IDD, exhibited significant differences in 20 subcategories of the ethogram (see Table 3). The subcategories of echolalia, rock, and spin were observed only in the ASD group (n = 8).

Table 2.

Subcategories that did not differentiate ASD and IDD

	ASD (n = 61)		IDD (n = 61)		p-value

	Mean	SD	Mean	SD
Point events
Automanipulation	6.3	5.1	7.1	5.0	0.355
Cover eyes	1.2	2.3	0.2	0.4	0.080
Hide	0.4	0.9	0.3	0.9	0.740
Laugh	0.6	2.1	0.4	1.0	0.366
Play (−)	0.8	2.2	0.4	1.4	0.416
Touch Psychiatrist	0.2	0.8	0.3	0.8	0.656
Touch Researcher	0.1	0.4	0.3	0.1	0.397

Lasting events
Far Away Researcher	9.6	4.4	10.1	5.7	0.210
Medium Researcher	3.9	4.2	4.4	5.4	0.953
Near Psychiatrist	1.6	2.5	2.3	3.9	0.680
Side Researcher	4.4	3.2	5.0	4.5	0.864

Table 3.

Subcategories that differentiate ASD and IDD in the unclassified group (n = 24)

	ASD (n = 8)		IDD (n = 16)		p-value

	Mean	SD	Mean	SD
Age	8.8	3.5	11.4	3.8	0.140

Point events
Approach	0.6	0.7	2.1	1.8	0.022
Turn Around	3.7	2.0	1.5	1.5	0.009
Vocalization	5.6	3.7	0.8	0.8	<0.001
Scream	1.1	1.3	0.1	0.3	0.029
Smile (−)	1.6	1.5	0.4	0.5	0.024
Tilt	11.3	5.0	4.2	2.2	0.002
Face Away	6.8	3.7	2.6	1.7	0.009
Stare Psychiatrist	7.5	3.5	14.1	5.7	0.006
Look Mother	15.8	6.4	6.1	3.4	<0.001
Look Psychiatrist	15.6	7.0	5.6	4.4	0.003
Look Researcher	10.5	5.3	4.6	3.6	0.013
Take (+)	<0.1	<0.1	0.4	0.5	0.030
Manipulate (+)	<0.1	<0.1	0.7	0.9	0.019
Touch Researcher	0.3	0.5	<0.1	<0.1	0.010

Lasting events
Facing Psychiatrist	6.3	3.0	10.8	3.3	0.008
Side Psychiatrist	4.5	0.9	2.8	2.3	0.010
Backs Turned Psychiatrist	4.1	2.7	1.5	1.6	0.038
Backs Turned Researcher	8.6	2.5	5.9	2.4	0.030
Medium Researcher	2.2	1.3	4.6	2.8	0.038
Far Away Researcher	11.8	1.8	8.0	3.8	0.028

The factor analysis of the ethogram's behavioral elements yielded a model with 24 factors, accounting for 79.3% of the variance. Table 4 gives an overview of the factor values and explains the variance and the internal consistency of the instrument. Four factors were identified based on eigenvalues and on the scree plot test, and these accounted for 37.6% of the variance. Thirty behavioral elements were excluded as they showed communalities below 0.4 or presented high factor loadings on two or more factors. Each of the four factors was named according to recognizable common features of the highest-loading behavioral elements. The factors were named as follows: Factor 1, General Movements (GM); Factor 2, Functional Communication (FC); Factor 3, Interpersonal Discomfort (ID); Factor 4, Stereotyped Behaviors (SB). Significant differences were found between the ASD and IDD patients in all four factors (p > .01). In relation to the IDD group, the ASD group had significantly higher scores on General Movements, Interpersonal Discomfort and Stereotyped Behaviors and presented significantly lower scores on Functional Communication.

Table 4.

Principal components analysis after Varimax rotation (n = 122)

Behavioral Elements	Factor loading by component

	GM	FC	ID	SB
Stand	0.840
Walk	0.758
Backs Turned Psychiatrist	0.740
Withdrawal	0.723
Approach	0.712
Backs Turned Researcher	0.696
Near Researcher	0.634
Turn Around	0.606
Explore (−)	0.599
Sit Down	0.596
Far Away Psychiatrist	0.540
Climb	0.539
Heteroagression	0.472
Far Away Mother	0.461
Scream	0.427
Head Spin	0.414
Facing Researcher	−0.415
Near Mother	−0.460
Side Mother	−0.534
Medium Psychiatrist	−0.609
Facing Psychiatrist	−0.660
Sit	−0.853
Point (+)		0.737
Smile (+)		0.723
Show (+)		0.669
Talk		0.668
Stare Mother		0.662
Mental State Language		0.661
Gaze Following		0.602
Shake		0.566
Facing Researcher		0.546
Ask		0.544
Nod		0.542
Near Psychiatrist		0.517
Answer		0.461
Smile (−)			0.629
Grimace			0.581
Rock			0.515
Look Mother			0.500
Tilt			0.441
Finger			0.436
Look Psychiatrist			0.411
Cover Eyes			0.405
Automanipulation			0.403
Explore (+)			−0.438
Give (+)			−0.448
Take (+)			−0.505
Play (+)			−0.523
Manipulate (+)			−0.573
Echolalia				0.757
Manipulate (−)				0.684
Lie Down				0.677
Play (−)				0.643
Sing				0.601
Look Own Object				0.484
Flapping				0.455
Laugh				0.440
Lying				0.427
Give (−)				0.418
Variance %	20.94	7.54	4.65	4.50
Cumulative	37.63
Cronbach's alpha	0.940	0.914	0.823	0.865
Total	0.868

Note: GM = General Movements; FC = Functional Communication; ID = Interpersonal Discomfort; SB = Stereotyped Behaviors

The binary logistic regression with the ethogram's factors showed that Functional Communication and Interpersonal Discomfort were significant predictors of ASD (see Table 5). A second logistic regression with the ethogram's main categories showed that Head Postures, Stare, and Look were significant predictors of the ASD (see Table 6). The predictive success of a diagnosis of ASD in the two logistic regression models was 98.4% and 95.9%, respectively. Due to problems of multicollinearity or singularity, lasting-event categories were removed from logistic regression analyses. The Hosmer-Lemeshow goodness-of-fit statistic (Hosmer and Lemeshow, 2000) was p > 0.05 in all steps of both logistic regression analyses.

Table 5.

Stepwise binary logistic regression analysis of the ethogram's factors predicting ASD (n = 122)

Explanatory Variables	B	SE	p-value	OR	95% CI
Initial Step
General Movements	0.678	0.686	0.323	1.969	0.513–7.556
Functional Communication	−1.044	0.496	0.035	0.352	0.133–0.932
Interpersonal Discomfort	2.337	1.223	0.056	10.351	0.943–113.655
Stereotyped Behaviors	1.005	0.670	0.134	2.731	0.735–10.148
Constant	−20.696	12.508	0.098	<0.001	-----

Final Step
Functional Communication	−1.160	0.558	0.038	0.313	0.105–0.936
Interpersonal Discomfort	1.877	0.866	0.030	6.532	1.195–35.694
Stereotyped Behaviors	1.102	0.713	0.122	3.009	0.744–12.172
Constant	−14.305	8.392	0.088	<0.001	-----

Notes: B = Partial regression coefficient; SE = Standard Error; OR = Odds ratio; 95% CI = 95% Confidence interval; Significant values in bold.

Table 6.

Stepwise binary logistic regression analysis of the ethogram's major categories predicting ASD (n = 122)

Explanatory Variables	B	SE	p-value	OR	95% CI
Initial Step
Body Postures	0.052	0.056	0.355	1.053	0.944–1.176
Facial Expressions	−0.046	0.091	0.611	0.955	0.799–1.141
Motor Stereotypies	0.088	0.056	0.117	1.092	0.978–1.219
Head Postures	0.298	0.116	0.010	1.348	1.074–1.692
Gestures	0.007	0.047	0.876	1.007	0.918–1.105
Stare	−0.186	0.057	0.001	0.831	0.742–0.929
Look	0.053	0.026	0.043	1.054	1.002–1.109
Verbalizations	−0.016	0.043	0.710	0.984	0.904–1.071
Constant	−4.846	2.512	0.054	0.008	-----

Final Step
Motor Stereotypies	0.089	0.059	0.133	1.093	0.973–1.228
Head Postures	0.302	0.108	0.005	1.353	1.095–1.671
Stare	−0.177	0.051	<0.001	0.837	0.758–0.925
Look	0.060	0.025	0.017	1.062	1.011–1.116
Constant	−5.054	2.332	0.030	0.006	-----

Notes: B = Partial regression coefficient; SE = Standard Error; OR = Odds ratio; 95% CI = 95% Confidence interval; Significant values in bold.

Discussion

The primary goal of this study was to develop a new ethogram describing behavioral elements that emerge in the psychiatric assessment of children and adolescents with ASD and IDD. Other objectives were to verify that this ethogram could differentiate the ASD group from the IDD group and that it could reliably predict the ASD according to the new DSM-5 criteria. The results of this study should be regarded with some prudence as to their generalizability. After all, the observation time per participant was relatively brief (15 minutes). Moreover, video recordings were performed only in one context of social interaction, they were coded by one observer who was not blind to the children's diagnoses, the participants received psychotropic medication, and there was no direct comparison with regard to predictive power between the ethogram and standard ratings. Nevertheless, the data presented here are sufficiently robust for an exploratory study.

We developed an ethogram covering a broad range of verbal and nonverbal behaviors of ASD and IDD, comprising earlier findings in classical ethological studies, and covering contemporary models of social behavior in mental disorders. Our ethogram not only precisely described the signs and symptoms of ASD, but also correctly classified ASD in most cases and clearly distinguished it from IDD, a developmental disorder that is common in childhood and adolescence. Furthermore, some subcategories of the ethogram that were related to gaze behavior, interpersonal distance, and avoidance behavior were able to differentiate children and adolescents with ASD and IDD who could not be categorized according to standard diagnostic checklists. A comparison between ASD and IDD on the behavioral elements of the ethogram revealed significant differences in: classic ASD behaviors, such as motor stereotypies (e.g., rock, hand-flapping), language stereotypies (e.g., echolalia), social interaction deficit (e.g., withdrawal, turn around), and gaze aversion (e.g., face away) (American Psychiatry Association, 2000; Kanner, 1943, 1971; World Health Organization, 1992); behaviors that are deficient in ASD according to established theoretical models, such as symbolic play, gaze following, pointing (i.e., joint attention), and use of mental-state language (Baron-Cohen, 1989, 1994; Baron-Cohen, Leslie, and Frith, 1985; Mundy, Sigman, and Kasari, 1990; Tager-Flusberg, 1981; Wing, Gould, Yeates, and Brierly, 1977); atypical behaviors that have also been described in ethological studies with ASD, such as gaze and physical aversion, echolalia, and motor stereotypies (Hutt and Ounsted, 1970; Pedersen, Livoir-Petersen, and Schelde, 1989; Pedersen and Schelde, 1997; Richer and Coss 1976; van Engeland et al., 1985); and in the nonspecific behaviors of ASD, such as walk, climb, explore, take, give, look own body, vocalization, and cry. Although children with ASD differed from IDD, it is not certain that the same would be true for contrasts between ASD and other mental disorders (e.g., childhood-onset schizophrenia), since the observed pattern of nonverbal behavior may not be specific to ASD. Future studies could use this ethogram to distinguish ASD from other mental disorders, to detect ASD in the general population, or even to study other behavioral conditions - analogous to previous ethological research with obsessive compulsive disorder (Eilam, Zor, Fineberg, and Hermesh, 2012; Zor et al., 2009; Zor, Szechtman, Hermesh, Fineberg, and Eilam, 2011).

The observation method of children and adolescents with ASD by means of discrete video recording devices and further analysis with an ethogram is minimally invasive, inexpensive, affordable, requires only a few minutes of video recording, and it is potentially more accurate than the typical clinical diagnostic procedures. Another advantage of this method in relation to standard ratings is that it does not depend on the parents' report, on the language development of the child or adolescent with the ASD, or on direct observation of behaviors, which are all methods that may suffer due to their lack of accuracy, especially in contexts where socioeconomic and sociocultural deprivation is common, such as in developing countries. On the other hand, the retrospective analysis of video recordings is time-consuming, may demand more training than just consulting DSM-5, may require multiple coders for behaviors that are difficult to identify (e.g., gaze following, mental state language), and perhaps may not be practical in clinical settings. Nevertheless, there are various computer programs that facilitate work with ethograms (e.g., the commercial “Observer” by Noldus, and the freeware “J-Watcher”). For research purposes, it may be an objective and very powerful tool for the detailed study of the social behaviors of autistic children and adolescents.

Footnotes

Acknowledgements

We would like to thank our patients and their families for their participation. We also thank Valerie Miller, MD, for constructive and valuable comments that helped improve an earlier version of the manuscript.

Ethogram

I- Body Postures
Walk	Locomotion not directed to another person
Sit Down	Self-explanatory
Stand Up	Self-explanatory
Lie Down	Self-explanatory
Climb	The arms pull, and the legs push the body up. The child may also climb onto large chairs, tables, etc
Bow	To bend forward with the upper part of the body
Approach	The child walks toward a person (to be distinguished from accidental movements in the direction of a person)
Withdrawal	The child walks away from some person (to be distinguished from accidental movements away)
Turn Around	Turns whole body around its axis for at least 90°

II- Verbalizations

Ask	Posing questions to somebody
Answer	Verbal reaction to a question from somebody
Echolalia	Repeating part of sentence spoken by somebody
Vocalization	Producing an unintelligible sound with mouth
Laugh	Self-explanatory
Cry	Self-explanatory
Scream	Self-explanatory
Mental State Language	Use of words such as “think”, “know”, “believe”, “wish”, “mean”, “pretend”, “forget”, “guess”, “want”, “believe”, “feel”, etc. (See Tager-Flusberg, 1981)
Talk	Using speech, loudly or quietly, other than as described

III- Facial Expressions

Smile (−)	The corners of the mouth are drawn back. The mouth is closed or slightly open. Does not establish eye contact
Smile (+)	The corners of the mouth are drawn back. The mouth is closed or slightly open. Establishes eye contact
Grimace	A sharp contortion of the face expressive of pain, contempt or disgust

IV- Motor Stereotypies

Rock	Rhythmic up-and-down movements, either in a lateral or dorsal-ventral way
Flapping	Stereotyped hand-flapping
Jump	Abruptly raises body with or without feet leaving the floor. Does not include skipping, galloping or dancing
Tiptoe	The child walks on toes
Clap	Claps hands repetitively out-of-context
Finger	Moves fingers in a flicking motion, often near the head
Spin	Rotating the body around its own axis repetitively and out-of-context

V- Head Postures

Nod	Moves head up and down, once or several times, quickly or slowly
Shake	Rotates head from side to side, between once and several times
Tilt	Tilts head forward, backwards, or sideways
Face Away	Turns face away from the partner more than 90°
Head Spin	Rotates the head around its own axis repetitively and out of context

VI- Stare

Stare Mother	Looks towards eyes of mother
Stare Psychiatrist	Looks towards eyes of psychiatrist
Stare Researcher	Looks towards eyes of researcher

VII- Look

Look Mother	Gaze directed to the mother's body
Look Psychiatrist	Gaze directed to the psychiatrist's body
Look Researcher	Gaze directed to the researcher's body
Look Body	Gaze directed to own body
Look Own Object	Looks at an object that is being manipulated by self
Look Other Object	Looks at an object that is being manipulated by another person
Look Away	Gaze directed away from the other person. This category includes looking at the wall, floor, door, table, window, and chair
Gaze Following	Follows the direction of gaze, head posture, or gestures of other people, and consequently shares a common social point of visual reference

VIII- Gestures

Automanipulation	Manipulates own body, e.g. finger against teeth, picking nose or teeth, fumbling with fingers
Autoagression	Hurts own body, e.g., scratching skin, pulling the hair, biting hand, banging head against something
Heteroagression	Physically assaults another person, e.g., hair pulling, kicking, punching, biting, scratching
Point (−)	Indicates something discrete with fingers, hands or arm gestures. Does not establish eye contact
Point (+)	Indication of something discrete by mean of fingers, hand or arm gestures. Establishes eye contact
Show (−)	Shows objects. Does not establish eye contact
Show (+)	Shows objects. Establishes eye contact
Give (−)	Gives an object to another person. Does not establish eye contact
Give (+)	Gives an object to another person. Establishes eye contact
Take (−)	Picks up an object from another person. Does not establish eye contact
Take (+)	Picks up an object from another person. Establishes eye contact
Manipulate (−)	Extensive handling of objects in any way, exclusive of play. Does not establish eye contact
Manipulate (+)	Extensive handling of objects in any way, exclusive of play. Establishes eye contact
Play (−)	Handling objects, toys in a constructive or symbolic way. Does not establish eye contact
Play (+)	Handling objects, toys in a constructive or symbolic way. Establishes eye contact
Explore (−)	Explores the room without making eye contact, e.g., opens and closes the door and the window, pushes the wall, beats the floor with hands
Explore (+)	Explores the room while establishing eye contact, e.g., opens and closes the door and the window, pushes the wall, beats the floor with hands
Touch Mother	Touches the mother's body
Touch Psychiatrist	Touches the psychiatrist's body
Touch Researcher	Touches the researcher's body
Cover Eyes	Covers eyes with own hands
Cover Ears	Covers ears with own hands
Hide	Hides behind a chair, under the table, behind the gurney

IX- Current Status

Sit	Self-explanatory
Stand	Self-explanatory
Lying	Self-explanatory
Facing Mother	The child is facing the mother
Facing Psychiatrist	The child is facing the psychiatrist
Facing Researcher	The child is facing the researcher
Side Mother	The child is beside the mother
Side Psychiatrist	The child is beside the psychiatrist
Side Researcher	The child is beside the researcher
Backs Turned Mother	The child has his back to the mother
Backs Turned	The child has his back to the psychiatrist
Psychiatrist
Backs Turned	The child has his back to the researcher
Researcher

X- Interpersonal Distance

Near Mother	Distance between child and mother is between 0 and 0.5 meters
Near Psychiatrist	Distance between child and psychiatrist is between 0 and 0.5 meters
Near Researcher	Distance between child and researcher is between 0 and 0.5 meters
Medium Mother	Distance between child and mother is between 0.5 and 1.5 meters
Medium Psychiatrist	Distance between child and psychiatrist is between 0.5 and 1.5 meters
Medium Researcher	Distance between child and researcher is between 0.5 and 1.5 meters
Far Away Mother	Distance between child and mother is more than 1.5 meters
Far Away Psychiatrist	Distance between child and psychiatrist is more than 1.5 meters
Far Away Researcher	Distance between child and researcher is more than 1.5 meters

Ethogram's scoring sheet for point events

ALL OCCURRENCES (Intervals in minutes)
Point Events	0–1	3–4	6–7	9–10	12–13	Total
Walk
Sit Down
Stand Up
Lie Down
Climb
Bow
Approach
Withdrawal
Turn Around
BODY POSTURES	-	-	-	-	-
Ask
Answer
Echolalia
Vocalization
Laugh
Cry
Scream
MS Language
Talk
VERBALIZATIONS	-	-	-	-	-
Smile (−)
Smile (+)
Grimace
FACIAL EXPRESSIONS	-	-	-	-	-
Rock
Flapping
Jump
Tiptoe
Clap
Finger
Spin
MOTOR STEREOTYPIES	-	-	-	-	-
Nod
Shake
Tilt
Face Away
Head Spin
HEAD POSTURES	-	-	-	-	-
Stare Parents
Stare Psychiatrist
Stare Researcher
STARE
Look Parents
Look Psychiatrist
Look Researcher
Look Body
Look Own Object
Look Other Object
Look Away
Gaze Following
LOOK	-	-	-	-	-
Automanipulation
Autoagression
Heteroagression
Point (−)
Point (+)
Show (−)
Show (+)
Give (−)
Give (+)
Take (−)
Take (+)
Manipulate (−)
Manipulate (+)
Play (−)
Play (+)
Explore (−)
Explore (+)
Touch Parents
Touch Psychiatrist
Touch Researcher
Cover Eyes
Cover Ears
Hide
GESTURES	-	-	-	-	-

Ethogram's scoring sheet for lasting-event categories

SCAN SAMPLING (Intervals in minutes)
Lasting Events	1	2	3	4	5	6	7	8	9	10	11	12	13	14	15	Total
Sit
Stand
Lying
Facing Mother
Facing Psychiatrist
Facing Researcher
Side Mother
Side Psychiatrist
Side Researcher
Backs Turned Mother
Backs TurnedPsychiatrist
Backs Turned Researcher
CURRENT STATUS	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-
Near Mother
Near Psychiatrist
Near Researcher
Medium Mother
Medium Psychiatrist
Medium Researcher
Far Away Mother
Far Away Psychiatrist
Far Away Researcher
INTERPERSONAL DISTANCE	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-	-

References

Altmann

(1974). Observational study of behavior: Sampling methods. Behavior, 49, 227–267.

American Psychiatric Association (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Publishing.

American Psychiatric Association (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Washington, DC: American Psychiatric Publishing.

Baron-Cohen

(1989). Perceptual role taking and protodeclarative pointing in autism. British Journal of Developmental Psychology, 7, 113–127.

Baron-Cohen

(1994). How to build a baby that can read minds: Cognitive mechanisms in mindreading. Cahiers de Psychologie Cognitive, 13, 513–552.

Baron-Cohen

(2009). Autism: The empathizing-systemizing (E-S) theory. Annals of the New York Academy of Sciences, 1156, 68–80.

Baron-Cohen

Leslie

, and Frith

(1985). Does the autistic child have a “Theory of Mind”? Cognition, 21, 37–46.

Burgemeister

B. B.

Blum

L. H.

, and Lorge

(2011). Escala de maturidade mental Colúmbia: Manual para aplicação e interpretação. (3rd ed.). São Paulo, SP: Casa do Psicólogo.

Castell

(1970). Physical distance and visual attention as measures of social interacting between child and adults. In Hutt

S. J.

and Hutt

(Eds.), Behavior studies in psychiatry (pp. 91–102). Oxford: Pergamon Press.

10.

Cattell

R. B.

(1966). The scree test for the number of factors. Multivariate Behavioral Research, 1, 629–637.

11.

Chiang

H. M.

(2008). Communicative spontaneity of children with autism: A preliminary analysis. Autism, 12, 9–21.

12.

Chiang

H. M.

(2009). Naturalistic observations of elicited expressive communication of children with autism. Autism, 13, 165–178.

13.

Churchill

D. W.

, and Bryson

(1972). Looking and approach behavior of psychotic and normal children as a function of adult attention or preoccupation. Comprehensive Psychiatry, 13, 171–177.

14.

Eibl-Eibesfeldt

(1989). Human Ethology. New York: Aldine de Gruyter.

15.

Eilam

Zor

Fineberg

, and Hermesh

(2012). Animal behavior as a conceptual framework for the study of obsessive-compulsive disorder (OCD). Behavioural Brain Research, 231, 289–296.

16.

Hosmer

D. W.

, and Lemeshow

(2000). Applied logistic regression (2nd ed.). New York: Wiley.

17.

Huerta

, and Lord

(2012). Diagnostic evaluation of autism spectrum disorders. Pediatric Clinics of North America, 59, 103–111.

18.

Hutt

, and Ounsted

(1970). Gaze aversion and its significance in childhood autism. In Hutt

S. J.

and Hutt

(Eds.), Behavior studies in psychiatry (pp. 103–120). Oxford: Pergamon Press.

19.

Jones

C. D.

, and Schwartz

I. S.

(2009). When asking questions is not enough: An observational study of social communication differences in high functioning children with autism. Journal of Autism and Developmental Disorders, 39, 432–443.

20.

Kanner

(1943). Autistic disturbances of affective contact. Nervous Child, 2, 217–250.

21.

Kanner

(1971). Follow-up study of eleven autistic children originally reported in 1943. Journal of Autism and Childhood Schizophrenia, 1, 119–145.

22.

Klein

(2000). The ethological approach to the study of human behavior. Neuroendocrinology Letters, 21, 477–481.

23.

Lorenz

(1974). Analogy as a source of knowledge. Science, 185, 229–234.

24.

Macintosh

, and Dissanayake

(2006). A comparative study of the spontaneous social interactions of children with high-functioning autism and children with Asperger's disorder. Autism, 10, 199–220.

25.

Mundy

Sigman

, and Kasari

(1990). A longitudinal study of joint attention and language development in autistic children. Journal of Autism and Developmental Disorders, 20, 115–127.

26.

Nazeer

, and Ghaziuddin

(2012). Autism spectrum disorders: Clinical features and diagnosis. Pediatric Clinics of North America, 59, 19–25.

27.

O'Connor

, and Hermelin

(1967). The selective visual attention of psychotic children. Journal of Child Psychology and Psychiatry, 8, 167–179.

28.

Pedersen

Livoir-Petersen

M. F.

, and Schelde

J. T. M.

(1989). An ethological approach to autism: An analysis of visual behavior and interpersonal contact in a child versus adult interaction. Acta Psychiatrica Scandinavica, 80, 346–355.

29.

Pedersen

, and Schelde

(1997). Behavioral aspects of infantile autism: An ethological description. European Child and Adolescent Psychiatry, 6, 96–106.

30.

Pereira

Riesgo

R. S.

, and Wagner

M. B.

(2008). Childhood autism: Translation and validation of the Childhood Autism Rating Scale for use in Brazil. The Journal of Pediatrics, 84, 487–494.

31.

Reser

J. R.

(2011). Conceptualizing the autism spectrum in terms of natural selection and behavioral ecology: The solitary forager hypothesis. Evolutionary Psychology, 9, 207–238.

32.

Richer

J. M.

, and Coss

R. G.

(1976). Gaze aversion in autistic and normal children. Acta Psychiatrica Scandinavica, 53, 193–210.

33.

Richer

J. M.

, and Richards

(1975). Reacting to autistic children: The danger of trying too hard. British Journal of Psychiatry, 127, 526–529.

34.

Setz

E.Z.F.

(1991). Métodos de quantificação de comportamento de primatas em estudos de campo. In Rylands

A. B.

and Bernardes

A. T.

(Eds.), A primatologia no Brasil (pp. 411–435). Belo Horizonte: Fundação Biodiversitas.

35.

Sokal

R. R.

, and Rohlf

F. J.

(1995). Biometry: The principles and practice of statistics in biological research (3rd ed.). New York: W. H. Freeman.

36.

Tager-Flusberg

(1981). On the nature of linguistic functioning in early infantile autism. Journal of Autism and Developmental Disorders, 11, 45–56.

37.

Tinbergen

(1974). Ethology and stress diseases. Science, 185, 20–27.

38.

Tinbergen

E. A.

, and Tinbergen

(1972). Early childhood autism: An ethological approach. Berlin: Parey.

39.

Troisi

(1999). Ethological research in clinical psychiatry: The study of nonverbal behavior during interviews. Neuroscience and Biobehavioral Reviews, 23, 905–913.

40.

Van Engeland

Bodnàr

F. A.

, and Bolhuis

(1985). Some qualitative aspects of the social behavior of autistic children: An ethological approach. Journal of Child Psychology and Psychiatry, 26, 879–893.

41.

Wechsler

(2002). Escala de inteligência Wechsler para crianças: Adaptação e padronização de uma amostra brasileira (3rd ed.). São Paulo, SP: Casa do Psicólogo.

42.

Wechsler

(2004). Escala de inteligencia Wechsler para adultos: Adaptação e padronização de uma amostra brasileira (3rd ed.). São Paulo, SP: Casa do Psicólogo.

43.

Wing

Gould

Yeates

S. R.

, and Brierly

L. M.

(1977). Symbolic play in severely mentally retarded and in autistic children. Journal of Child Psychology and Psychiatry, 18, 167–178.

44.

Wing

, and Ricks

D. M.

(1976). The aetiology of childhood autism: A criticism of the Tinbergens' ethological theory. Psychological Medicine, 6, 533–543.

45.

World Health Organization. (1992). The ICD-10 classification of mental and behavioral disorders: Clinical descriptions and diagnostic guidelines. Geneva, Switzerland: World Health Organization.

46.

Zabel

, and Zabel

(1982). Ethological approaches with autistic and other abnormal populations. Journal of Autism and Developmental Disorders, 12, 71–83.

47.

Zar

J. H.

(1998). Biostatistical Analysis (4th ed.). Upper Saddle River, NJ: Prentice-Hall.

48.

Zor

Keren

Hermesh

Szechtman

Mort

, and Eilam

(2009). Obsessive-compulsive disorder: A disorder of pessimal (non-functional) motor behavior. Acta Psychiatrica Scandinavica, 120, 288–298.

49.

Zor

Szechtman

Hermesh

Fineberg

N. A.

, and Eilam

(2011). Manifestation of Incompleteness in Obsessive- Compulsive Disorder (OCD) as Reduced Functionality and Extended Activity beyond Task Completion. PLoS ONE, 6, e25217.