Insights from pioneers of autism

Several years before both Kanner's and Asperger's works, a Russia's leading female child psychiatrist had already described this type of children. Grunja Sukhareva’s centenary papers were recently translated in english journals and have beene the focus of a recent paper on IJP by Liliana Dell'Osso who proposed that the recent concept of female ‘camouflaging’ was already present in those papers. Here we reconsider female camouflaging and its relation with imitation, coping and emotional dysregulation. In addition we focus on other specific sex-related characteristics described by Sukhareva: the less pronounced schizoid nature of thinking; the less pronounced motor symptoms, especially expressive movements and facial expressions, and negativism.

Article

Three of the eleven children described in what is historically considered the seminal work of infantile autism ¹ were girls. Barbara, case no. 5, 8 years old, is described as a skilled reader despite her verbal language difficulties. Virginia, case no. 6, 11 years old, is a tall, slender girl, very neatly dressed and adept at puzzles solving, whose mutacism is interpreted by Kanner as an expression of a personality disorder rather than an organic impairment; Virginia’s non-verbal IQ is reported as 94 but ‘without a doubt her intelligence is higher than this score’, Kanner writes. Elaine, case no. 11, aged 7, is described as hypersensitive and endowed with a special language such as: ‘there is war in the sky’. Three girls out of eleven, i.e. 27%, one girl for every three/four boys: therefore, why autism was subsequently considered a male disorder which, if already rare in this sex, was believed to be even rarer in females and frequently burdened by the association with significant cognitive deficits?

A vision of autism as a severe male disturbance (and even more rare and severe in females), clearly not present in Kanner’s original description, was further supported in 1981, when Lorna Wing ² made known to the English-speaking world the paper published in German by Hans Asperger in 1944 on the autistic psychopathy ³. The fact that the four children described in the original Asperger’s paper, later translated by Uta Frith (1991), were all boys, seemed to confirm that autism was exceptional in girls, despite Lorna Wing had been motivated in its dissemination work by being the mother of a little girl with behaviors similar to those of the children described by Asperger.

It is now known that several years before both Kanner’s and Asperger’s works, a Russia’s leading female child psychiatrist had already described this type of children. In this case, we owe Sula Wolff the merit in 1996 of having made known to the English-speaking world the work published by Grunja Sukhareva exactly seventy years earlier Kanner and Asperger investigations ⁴. Grunja Sukhareva described six male children, which presented what she called ‘schizoid psychopathy’ and who were similar in every way to the four male children characterized in the Asperger’s work. We can suppose that also in this translation the ‘male’ preconception have played a role. Indeed, it still took more than twenty years for an autistic woman ⁵, a professional translator, to realize that Grunja Sukhareva’s original work was composed of two parts, the second of which had been omitted by Sula Wolff. Simmonds translated and published this second part of Sukhareva’s paper, where she describes five girls, which seem to be on the autistic spectrum. This contribution not only shed light on the role of female researchers in the history of autism, but it is also crucial to fill the existing gap in the literature on autism in girls and women. Indeed, the second part of the Sukhareva work testified her conviction, which did not concern the two ‘male’ researchers Kanner and Asperger, that ‘the problem of the influence of sex differences on the symptomatology and course of various clinical forms deserves much more attention than it usually receives’.

Liliana Dell’Osso and her group ⁶ was therefore right to underline the importance of this pioneer of European child psychiatry, and to place her work at the core of the current, and thankfully no longer neglected reflections on autism in girls, adolescents and women. The literature on this topic is now very extensive although with somewhat conflicting results. However, according to recent research reviews, some sex-specific differences in the autistic clinical presentation were reported. In particular, compared to males with ASD, females with ASD show significantly better social interaction and social communication skills, fewer stereotyped behaviours and restricted interests, more internalizing problems (anxiety, depression, and eating disorders) ^7-9. These symptoms are at least partly supported by different genetic substrate ¹⁰ and neuroanatomy ¹¹ that characterize males and females with ASD. For instance, as far as the neuroanatomical underpinnings, a large clinical and brain-imaging study identified a subgroup of children, predominantly female, characterized by increased emotional-behavioral problems and a larger right amygdala, suggesting a specific brain-behavior correlation in at least a subset of autistic girls ¹². On the other hand, Lee et al. ¹³ reported a rate of disproportionate megalencephaly twice high in boys compared with girls.

Returning to the topic of Grunja Sukhareva’s clinical insights on autism in females, we will analyze this aspect starting from the Liliana Dell’Osso’s editorial, which specifically focuses on the mechanism described in the current literature as ‘camouflaging’ ¹⁴. Specifically, in the ASD field, the term camouflaging has been used to refer to the process by which subjects with ASD hide or mask features that may be considered as socially inappropriate, and/or artificially perform behaviors deemed to be more socially acceptable ¹⁵. Dell’Osso et al. ⁶ suggested that the decrease in mood instability with age reported in Sukhareva’s cases, with girls becoming “softer and calmer” over time, could be ascribed to the gradual learning of camouflage strategies. Once implemented, these strategies could result in phases of increased behavioral calm and apparent mood stability. Thus, the girls described by Sukhareva may have become more proficient at using these strategies, creating, over time, the impression of stable mood and emotional regulation. Therefore, according to Dell’Osso and colleagues ⁶, in the discerning clinical reports by Sukhareva’s centenary writings, it is possible to glimpse what after a hundred years the most recent edition of DSM-5 states ¹⁶ regarding the typical and voluntary modification of autistic behavior based on the social context to which the autistic girl is exposed. While autistic males can react to stress and social pressures through an increase of repetitive behaviours, autistic girls tend to mask their symptoms, mimicking behaviors they deem appropriate based on societal expectations. As a consequence, autistic females without language or intellectual disability may not receive an ASD diagnosis or receive a misdiagnosis due to camouflaging, with a negative impact both on tailored treatment and outcome ^17-18. However, camouflage requires constant effort in order to actively try to mask and compensate for the autistic characteristics, and therefore can also lead to a mental, physical and emotional exhaustion, exacerbating some internalizing behaviors, including depression, anxiety, and a grater risk for suicide ²⁰. Thus, internalizing behaviors in autistic girls may be associated with camouflaging adaptations. In this regard, the DSM-5 calls into question ‘coping’ mechanisms (in the sense of ‘copying’ and not ‘coping’). In our opinion, it is important to preserve this term without confusing it with the imitation. Indeed, the discovery of mirror neurons in several animal species (for a recent review, see ²¹) revealed that observation and action have common neural underpinnings, and imitation has become a fundamental mechanism for the development of social relationships. On the other hand, psychoanalysis had already considered imitation and introjection as constitutive elements of the identification process ²². Specifically, in the identification process, imitations and introjections are fused and integrated with the aim of adapting to reality. Imitation is essential for identification as is introjection, but imitation and introjection should be distinguished. We could hypothesize that in the camouflaging mechanism there is an imitation without introjection, giving rise to a sort of mimicry rather than identification. Probably because of this aspect, the clinical picture of autistic female, in which camouflaging is more frequent ^23,24, is often accompanied by affective disorders, including ambivalence of emotions, emotional eccentricity, insufficient affective responses, volatility of mood, presence of complicated and contradictory emotional combinations. Some recent investigations reported this frequent comorbidity: for instance, Remnélius & Bolte ²⁵ described a direct correlation between camouflaging and depressive symptoms. Wieckowski ²⁶ examining gender differences in emotion regulation in autistic male and female aged 4-20 years found that autistic females had more severe dysregulation, including higher reactivity and dysphoria, which increased with age.

In addition to the more frequent emotional dysregulation, other specific sex-related characteristics have been described by Sukhareva in ASD females ⁴: the less pronounced schizoid nature of thinking, the less pronounced motor symptoms, especially expressive movements and facial expressions, and negativism that ‘can be seen more frequently in girls and always has a hysteroid quality’. We will focus on the last two characteristics.

Sukhareva had already placed motor disorders among the main features of autism in her six autistic males. To our research group that has long been focused on early atypical motor organization in autism (the studies are now summarized in an Italian book) ²⁷, this aspect looks like an intuition that is still waiting to be fully recognized. It is no coincidence that the motor atypicalities, although frequently reported in the ASD population ^28,29, are not yet present among ASD characteristics in the classification systems, in which motor problems are considered a negligible element of autism, without any influence on diagnosis and intervention. Conversely, Sukhareva farsightedly supported the “theory that explains the autistic disposition of the schizoid children through their motor skill deficits: the awkwardness of their movements makes them fearful and shy, compels them to avoid interaction with people...in the schizoid psychopathies motor skill deficit, that are present from birth, could have great significance for the development of social attitude…we have observed motor symptoms in all our cases”. In this framework, past studies demonstrated that motor and social communication abilities are strictly connected in ASD ³⁰. In giving importance to the motor functions and their close link with the social world, the Sukhareva’s work has important aspects in common with that of George Frankl, another pioneer of autism who was underestimated until very recent years ³¹. Frankl’s idea ³² was that autism is characterized by an impairment in emotional (body) language: while in neuro-typical subjects, everyday language is always an integration of emotional (non-verbal) and verbal language, autistic children experience a rupture between them, which is the essence of autism. In fact, affective language for Frankl is not only a non-verbal language, but it is a motor-corporeal language in the broadest sense. We think that autism as an affective language disorder is consistent with the DSM-5’s creation of a socio-communicative domain that includes only non-verbal communication (affective language), placing verbal language (word language) as a ‘specifier’, and not as a diagnostic criterion. In this regard, Dell’Osso rightly refers to the DSM-5-TR, which reports the presence in autistic females of a integration between verbal and non-verbal behavior, and also notes how these better abilities at the level of expressive movements in females compared with matched males were already been reported by Sukhareva.

According to Sukhareva, the other differential element between males and females with ASD is negativism. Hence, in her descriptions of all the five girls ³³, terms such as strong-willed and stubborn, unmanageable, disobedient, rough and sometimes even cruel, intolerant of refusals when she wanted something, full of negativistic responses, obstinate negativism, rude, insolent, undisciplined, cheeky, blunt, not compliant with rules, difficult girl, continually recurred. Sukhareva summarized these behavioral characteristics with the term ‘negativism’, and observed that such features are more frequently present in girls than in boys. Therefore Sukhareva considered greater levels of negativism as one of the differential features of schizoid (term that she subsequently replaced with ‘autistic’) psychopathies in girl. Even in this field Sukhareva’s contribution proves far-sighted. Firstly because she brings to the fore cognitive aspects such as inflexibility and the hyperbolic sense of justice, which have been described as characteristic of the autistic functioning. Second, the nature of the externalizing behaviors described by Sukhareva are very different from those of an oppositional conduct disorders with which autistic stubbornness, linked to inflexibility, can easily be confused ³⁴. Third, because Sukhareva breaks what is proving to be a misconception, namely that autistic girls experience more internalizing behaviors in comparison to autistic boys, whereas autistic boys exhibit more externalizing behaviors than autistic girls. This clinical insight is confirmed by different recent studies. Specifically, Holtmann et al. ³⁵ found that girls, matched for communication difficulties and IQ with boys, exhibited not only more emotional dysregulation but also higher scores on externalizing behaviors than male peers. Similar results are reported in a recent investigation ³⁶, and interpreted as a possible negative behavioral consequence of exhausting camouflaging strategies more frequent in ASD females than in ASD males ³⁷.

So why talk about pioneers? Returning to the history of autism allows the clinician to situate himself among generations of visionary predecessors, grappling with something unknown that challenged them. It is following in the footsteps of our pioneers and keeping an open mind away from the simplifications often induced by a complex and still enigmatic topic like autism. Studying their almost century-old works revives the phenomenological approach and the pleasure of reading detailed descriptions of children interacting with the world, accompanied by a respectful attempt to understand behavior, a clinical attitude that seems to disappear in the current scientific literature predominantly based on large numbers. It could be thought that if the work of Sukhareva and Frankl had been more successful, the enormous ambiguities that have characterized the history of autism as a male disturbance might have been attenuated. In her PhD dissertation, Simmonds ³⁸ has opined that ‘the Anglo-European world’ was left almost 100 years behind Russia in recognising the ‘female autism phenotype’, and that misogyny likely contributed to preventing greater reputation for Sukhareva’s perspicacious investigations on sex differences in autism. Can we think that this time is over?