Abstract
Behavioural observation of psychiatric patient groups using ethological methodology has never been a mainstream approach in psychiatry. In the present review article it is argued that the assessment of non-verbal behaviour in psychiatric disorders has much to offer to clinicians. Based on a Medline survey, the literature on ethological observation of patients with depression and schizophrenia was reviewed. Ethological observation of psychiatric patient groups has the potential to improve prediction of course and outcome of severe psychiatric disorders at a very early stage. Disadvantages of the ethological approach lie within its technical requirements and its inherent time-consuming evaluation of data. A full appreciation of psychiatric disorders may require answers to questions to the proximate causes and evolutionary (Darwinian) trajectories of behaviour, an approach that may well be expanded to maladaptive cognition and emotion.
Ethology, as conceptualized in a seminal paper by Nico Tinbergen on the occasion of Konrad Lorenz' 60th birthday, deals with the causation, ontogeny, survival value and evolutionary trajectories of behaviour [1]. The first two of these so-called ‘why’ questions concern the proximate causes of behaviour, which pertain to the processing of internal and external stimuli (physiology), and the ontogenetic development of behaviours over an individual' lifespan. For example, questions related to ontogeny inquire how behaviour changes with ageing, and which early experiences are necessary for a given behaviour to develop properly. The other two questions, referred to as the ultimate causes, address the evolutionary processes that have shaped the behaviour. One question concerns the selective advantages or biological function of behaviour, which includes the analysis of how behaviour impacts on an individual' inclusive fitness (i.e. survival and reproductive success); the other traces the phylogeny of behaviour, which involves cross-species comparison of behaviour, and concerns how the behaviour might have arisen and how it was modified in the course of evolution [1]. Both the proximate and the ultimate causes are regarded as complementary in explanatory power of behaviour.
Traditionally, psychiatry overlaps with ethology regarding the search for proximate causes of behaviour (albeit psychiatry focuses on pathological variants). But even though leading scholars recognized the importance of behavioural observation from the very beginning of psychiatry as a medical discipline in the 19th century [2,3], ethological research based on modern evolutionary conceptualizations has received relatively little attention in the (recent) past. Likewise, psychiatry has largely disregarded the value of considering the evolved function of behaviour such that the messages of non-verbal patterns of behaviour are inadequately understood. Even more so, psychiatry has omitted the possibility that the four questions can be applied to emotional and cognitive processes as well.
A large part of non-verbal behaviour is out of conscious control. Facial expressions of emotion, gestures and body postures are by and large involuntary. As such, the information provided by the analysis of non-verbal behaviour may differ from the information via verbal report [4]. If, for example, a person tries to put on a friendly smile, even if he or she does not feel like that, the smile can easily be uncovered as a ‘fake smile’ by experienced observers, simply because voluntary control over the upper part of the face (eye region) is weak compared to the lower face [5].
The failure of psychiatry to categorize observable behaviours in a framework grounded in human (behavioural) biology has greatly hampered studies into diagnostic accuracy, treatment and prognosis of psychopathological conditions. For example, many experienced psychiatrists are well familiar with a vague feeling that something is wrong in a patient who is developing a psychotic disorder. This intuitive recognition of subtle abnormalities in behaviour, known as ‘praecox feeling’ [6], is widely believed to be a reliable tool in psychiatric examination [7], although it largely lacks scientific appreciation.
In spite of the ignorance of mainstream psychiatry, a handful of psychiatric research groups have built upon the new discipline of human ethology [8], which emerged as an extension of animal ethology in the second half of the 20th century. They basically suggest that ethological research in psychiatric patient groups not only can make a valuable contribution to psychiatry and to insights into psychopathology, but also to the construction of an empirically testable framework for the understanding of abnormal behaviours [9–16]. In the 1950s, for example, Staehelin carried out systematic observation of patients with chronic schizophrenia on the ward and recognized a marked autistic ‘a-sociality’ on the one hand, and the emergence of a strong pecking order or hierarchy on the other [17]. In the late 1950s and early 1960s, ethological research in psychiatric patient groups as well as with regard to a cross-species perspective was further advanced in the pioneering work of Ploog [10,18,19]. Ploog was among the first to highlight the similarities of stereotyped behaviours observed in chronic schizophrenia with instinctual behaviours in animals [18]. In a similar vein, the Tinbergen and Tinbergen analysis of the non-verbal behaviour of autistic children [20] has been a source of inspiration for several other ethological studies into various types of psychopathology, although their approach to autism was later refuted. Finally, the Bowlby attachment theory has become one of the most influential ethological theories in psychiatry [21,22]. One of the core ideas advanced in the Bowlby theoretical model is that early social interaction between mother and newborn plays a crucial role in the social development of the offspring later in life, and that anomalous early attachment experiences may predispose the child to psychopathology later in life. By now, this core idea is generally accepted and utilized in psychological and psychiatric clinical practice.
When looking at systematic behavioural observation in psychiatric patient groups it becomes evident that most studies have concentrated on two phenotypes of psychiatric disorders: depression and schizophrenia. The purpose of the present review, based on a Medline survey, was to summarize the most important findings from ethological observation in depression and schizophrenia. Accordingly, we deliberately excluded the extensive literature on facial expressions of emotion in both depression and schizophrenia, on which excellent reviews exist [23,24]; neither do we discuss in depth the vast literature on the impact of poor attachment on psychological problems. Instead, we will try to put forth the idea – or advocate its revival – that the understanding of psychopathology necessitates a full appreciation of all four questions raised by Tinbergen, that is, both proximate and ultimate factors.
Ethological analysis of behaviour
It is assumed that >60% of human communication is effected via non-verbal behaviour [23,25]. Thus, one can argue that an ethological analysis of psychiatric patients’ non-verbal interactions with others may indeed contribute to a better understanding of the role of interpersonal processes in the onset and course of the disorder.
A basic assumption that underlies the ethological analysis of behaviour is that the behaviour of the species under study is hierarchically organized. Several elements of behaviour may or may not share a common causal factor and a common (biological) function. That is, elements of behaviour that occur in the same context but not in others are assumed to share a similar cause that is related to this context. In addition, behavioural elements that produce a similar effect are assumed to be functionally homologous. Based on contextual evidence and consequential evidence, these elements are pooled into a higher-order factor. In turn, several higher-order factors together can constitute the behavioural repertoire that serves the achievement of a biological motivation (e.g. reproduction, territorial behaviour, social behaviour etc.). In the observation and registration of behaviour ethologists make use of ethograms. Ethograms are catalogues of discrete elements of behaviour that make part of the behavioural repertoire of the species under study. The behavioural elements that constitute an ethogram need to be sufficiently distinguishable from other elements of behaviour (i.e. sufficiently uniform and recurrent) in order to allow the registration of objective parameters (e.g. frequency and duration).
Most ethological studies into psychopathological conditions have used (variants of) an ethogram developed by Grant [26]. This ethogram focuses on the coding of human behaviour during interviews and consists of >100 different codable simple or complex movements such as eye-blink, gaze direction and facial movements, as well as body posture. These behavioural elements are allocated to one of four categories, namely Flight, Assertion, Contact, and Relaxation. For example, drawing back one' mouth corners represents an involuntary and unconscious expression of submission and is often motivated by a tendency to escape a situation. In contrast, an eyebrow flash invites social interaction [8] and is accordingly grouped with other affiliation signals as ‘contact’ behaviour [26,27]. In human interaction, elements that indicate motivational ambivalence, for example between flight and assertion, referred to as ‘displacement behaviours’ [28], occur frequently in clinical interview situations, and these elements can be observed across diagnostic categories. Based on Grant' ethogram and its variants as used by Polsky and McGuire, Schelde
In a similar vein, Bouhuys
Ethology of depression and schizophrenia
Several studies have investigated whether and how ethograms differ between psychiatric patients and healthy controls, and between patients with different types of psychopathology, respectively. McGuire and Polsky investigated whether ethological methods can be used to identify different types of psychopathology [29,35,36]. They observed behaviour of patients with depression (n = 6), schizophreniform disorder (n = 6), and personality disorder (n = 4) in semi-naturalistic settings on the ward. Patients with depression displayed non-social behaviours most frequently and invited others to social interaction less than patients with schizophrenia or personality disorders. They also found that during the time-course of hospitalization the interpersonal space between the patient and others changed in patients with schizophrenia and in patients with personality disorder, but not in depressed patients. Overall, the amount of social behaviour increased with clinical improvement [29]. Differences in observed social behaviour between patients who would improve and those who would not emerged in the second week of hospitalization. Behaviour as observed during the first week, however, did not predict subsequent clinical improvement. Fossi
In contrast to the semi-naturalistic ward observations, Jones and Pansa observed the behaviour of depressed patients (n = 23), schizophrenia patients (n = 20), and controls (n = 43) during a clinical interview at hospital admission [40]. Compared to healthy controls, depressed patients demonstrated both shorter durations and lower frequencies of smiling and looking at the interviewer. During the early phase of the interview, eye contact was also shorter than in patients with schizophrenia. Furthermore, when compared to patients with schizophrenia as well as to healthy controls, depressed patients demonstrated a shorter duration and lower frequency of body-focused hand movements. With clinical improvement, particularly the frequency and duration of smiles during the first 2 min of the interview increased. Jones and Pansa furthermore found that the time-course of the behaviour over the interview differed between depressed patients and those with schizophrenia [40]. Hence, in line with findings from ward observations, the findings from clinical interviews also point out that social behaviour distinguishes depressed patients from patients with schizophrenia and from healthy controls.
Troisi
Prediction of course and outcome in depression and schizophrenia based on non-verbal behaviour
The findings described in the previous section point to an association between disturbed non-verbal interpersonal behaviour and depression and schizophrenia. Further evidence that these disturbed non-verbal interactions play a causal role in depression and schizophrenia comes from studies that investigated whether disturbed non-verbal interactions can also predict the course of depression and schizophrenia. Ranelli and Miller investigated non-verbal behaviour of 18 depressed patients in relation to the course of depression over a 6 week follow up [43]. They found that patients who would not improve displayed a high frequency of body-focused adaptors, posture shifts and speech pauses. Patients who would improve displayed long speech pauses and head aversions. Using the ECSI, Troisi
Hale
Geerts
In healthy subjects, non-verbal convergence between conversation partners during an interaction underlies satisfaction with the interaction and mutual attraction [52,53]. In remitted depressed patients Geerts
Geerts and Bouhuys re-analysed the Hale
To summarize, behavioural observations of depressed patients during a clinical interview confirm findings from ward observation that impaired social behaviour is involved in depression. Moreover, in contrast to the ward observations, the non-verbal behaviour as registered from clinical interviews does predict the subsequent course of depression. This predictive quality is not restricted to the patients’ behaviour. Also, the behaviour of the conversation partner is associated with the subsequent course of depression. Ward observations have shown that depressed patients engage less often in social interactions. The observations of clinical interviews can be interpreted in terms of a measure of the quality of the interaction. Hence, a possible explanation of the difference in predictive quality between ward observations and those from clinical interviews is that the quality of social interactions plays a causal role in the onset and course of depression, more than the quantity of social interactions. This explanation is supported by findings that the interaction between the behaviour of patients and conversation partners is associated with the subsequent course of depression. Alternative explanations, however, are also possible. The number of patients who participated in the clinical interviews exceeds that of patients who were studies in the ward observations. Hence, the lack of predictive quality of ward observations may be a simple problem of lack of power. In addition, the circumstances of clinical interviews are more standardized than those of ward observations. This may also explain why behaviour as observed during clinical interviews does predict the course of depression whereas behaviour observed of patients on the ward does not.
In contrast to the number of studies on the predictive quality of observable behaviour with respect to the onset and course of depression, little is known on this predictive quality in patients with schizophrenia. Troisi
Discussion
In this article we have reviewed ethological naturalistic observational studies of depression and schizophrenia. We argue that Tinbergen' four questions that address the causes of behaviour at the proximate and the ultimate level [1] can be a useful and informative tool for behavioural observations in psychiatric patient groups and are a necessary tool for a full and comprehensive understanding of psychopathology in an evolutionary perspective, for several reasons. First, ethology helps categorize behaviours in terms of their communicative meaning. Drawing on cross-species as well as cross-cultural issues, behaviours observed in psychiatric patients can be put in an empirically testable framework. For example, behaviours seen in depression or schizophrenia such as crouching postures, averted gaze or displacement activities often reflect defensive strategies [67,68]. Accordingly, changing patterns of behaviour, for example observed in a patient who is able to engage less often in such defensive positions, can be linked to questions about clinical improvement, even before the patient (or clinician) becomes subjectively aware of it. More importantly, increase of displacement activities, if recognized, can alert clinicians to check for clinical deterioration. For example, such behaviour may indicate increasing motivational conflict and ambivalence, which can be a sign of impending suicidal behaviour [31]. These examples of behavioural analyses based on ethological methodology explicitly assume that behaviours found in clinical conditions are not qualitatively distinct from behaviours in healthy individuals but are different by degree, that is, intensity, frequency or contextual inappropriateness [41,69]. Second, behavioural observation is often much more reliable than subjective report, because it is much less under conscious control compared to verbal communication such that an individual' real motives cannot so easily be concealed [32]. For the very same reason, an ethological approach is at least as valuable as (evolutionary) psychological approaches based on questionnaires [70]. The studies cited here clearly demonstrate the usefulness of ethological observations in revealing the mechanisms that underlie the onset and course of disorders. Third, standard rating scales utilized in clinical assessments critically depend on the clinician' impression of patients’ non-verbal behaviour. Even though manuals available for clinical rating scales hardly ever recur on ethological theory, clinicians intuitively use their species-specific endowments for deciphering non-verbal expressions in therapist–patient interactions. The extent to which actual clinical judgements rely on unconsciously perceived communicative signals sent by patients compared to their subjective report is a highly underresearched topic in clinical psychiatry [41].
Ethological observation in psychiatric patient groups also has, however, a number of disadvantages. Ethological methodology is still outside psychiatric mainstream research, because it is extremely time-consuming, and because it requires training that medical or psychology students usually do not receive (because ethology is not part of the curriculum), thus, ethological terminology is unfamiliar to most clinicians. Moreover, behavioural observation in psychiatric patient groups has very rarely been linked with physiological measures such as neurotransmitter activity or genetic variation. These disadvantages ought to be overcome if psychiatry wants to survive as a medical discipline rooted in the natural sciences.
Apart from psychiatry, we also believe that ethology has much to offer to evolutionary psychology. As we have argued, an evolutionary explanation of psychopathology makes no sense if it does not fit with the empirically based findings on causation and ontogeny. Ethological studies may provide empirical data that can be used to test evolutionary explanations. For instance, the results of ethological observations together with findings from other studies that point to a decreased fitness in depression and findings that even mild signals of depression induce rejection in others [71] challenge evolutionary explanations that depression may be explained as a strategy to seek support and to decrease social threat [72]. In fact, empirical evidence exists that the non-verbal social behaviour of depression-prone people may generate the negative interpersonal events that in turn provoke depression [61]. We therefore assert that a comprehensive evolutionary approach of psychopathology requires the full exploration of all possible explanations of how these disorders may have been maintained in the human population over the course of evolution.
The study of psychiatric patient groups, in comparison to healthy controls, for instance, can identify important details of proximate and ultimate factors of human life. This way, ethology, sociobiology, and evolutionary psychology may return to the methodology of Darwin' ‘On the Expressions of Emotions in Man and Animals’, first published in 1872 [73]. Remarkably, Darwin drew heavily on facial expressions observed in patients with mental illnesses and included several pictures taken by Crichton-Browne, who later became one of the leading psychiatric authorities in Great Britain.
Focusing on non-verbal behaviour in psychiatric patient groups does by no means suggest that patients’ verbal report and subjective experiences are less important sources of information. Non-verbal behaviour, however, has grossly been neglected in psychiatric research in the past, compared to the subjective side of mental illness.
In any event, cognitive and emotional processes have an evolutionary history in essentially the same way that behaviour has. Accordingly, they should be analysed in exactly the same way as behaviour. It could therefore be a fruitful approach to combine research into cognitive deficits with that on non-verbal behaviour, as has recently been demonstrated by Brüne
