Joseph Polimeni

The crisis of psychiatry — insights and prospects from evolutionary theory

Darwin’s emphasis on natural selection has had a transformative influence on how biological and medical sciences are conceptualized and conducted. However, the relevance of his ideas for the understanding of psychiatric conditions is still under-appreciated. Modern understanding of disease has required appreciation of the dialectical give and take between environmental influences, life history theory imperatives, human behavioral ecology, and characteristics of adaptive processes at all levels of the individual. This has enabled a better comprehension of metabolic disturbances, cancers, auto-immune disease, inherited anemias, and vulnerability to infectious disease 1. Here we propose that a contemporary and scientifically satisfying understanding of psychiatric conditions requires adopting a similar logic of inquiry, by taking into consideration the influence of environmental contingencies and natural selection in sculpting not just brain based mechanisms and processes germane to clinical neurosciences, but also diverse characteristics of behavior. One approach to understand psychiatric disorders in an evolutionary perspective builds upon Nobel laureate Nikolaas Tinbergen’s ideas, suggesting that, for a full understanding of any given phenotypic trait, one needs to detect the development and nature of its mechanisms, construed as the “proximate causes”, and, in addition, its evolutionary (or phylogenetic) history and adaptive value 2. Studying the proximate mechanisms is standard in psychiatry and the clinical neurosciences, but the questions pertaining to the phylogeny of traits have largely been ignored. Admittedly, placing dysfunctional cognitive, emotional and behavioral processes in the context of possible adaptation is not straightforward at first sight. The clinical directive requires that “disorder” represent the appropriate focus. However, a “disorder” – by definition – is counter-intuitive in the context of adaptation. By adaptation we mean a genetically-mediated structural or behavioral trait, which when possessed, increased survival and reproductive success in the environment in which the trait evolved. Were psychiatry’s focus be placed on “traits” (i.e., cognitive processes, emotions, and behaviors), problems which are clinically relevant could more satisfactorily be understood as distorted expression of mechanisms that in earlier environments provided answers to problems of adaptive significance, but which currently interfere in light of prevailing environmental contingencies 3. Important to the understanding of a particular phenotype is the evolutionary concept of variation. Without variation, no evolution by natural selection could take place. Mainstream psychiatry has largely ignored the fact that variation is the rule, not the exception, and this creates conceptual tensions. Psychiatry conceptualizes “disorder” as a statistical deviation from a normative statistical mean, yet handles it as a category. In other words, both “normalcy” as well as “disorder” with regard to psychological or behavioral functioning are burdened with the connotation of low variation. Phenotypic variation is the result of a complex interplay of genotype and environment, including epigenetic mechanisms that are decisively shaped by experience over the individual lifespan. These issues translate to providing a clinician with a rationale for explaining why, how, and when adaptive behavior is compromised and constrained; that is, when social, cultural, or ecological conditions and circumstances pose hindrances or risks which interfere with achievement of best solutions to socio-biological problems, and which may require a modification of a strategy of coping, selection of an alternative strategy, and/or the setting of more realistic biological goals. This integrative view of psychopathology, we believe, can have profound effects on how psychiatry conceptualizes disorders, which shall be illustrated briefly in three examples.

Deficit in schizophrenia to recruit the striatum in implicit learning: A functional magnetic resonance imaging investigation

In schizophrenia, explicit learning deficits have been well established although it is less clear whether these patients have deficits in implicit learning (IL). IL is thought to depend on intact striatal functioning. This study examined the hypothesis that schizophrenia patients show deficient recruitment of striatal activation during an IL paradigm, relative to performance-matched healthy comparison subjects. Ten subjects with schizophrenia on atypical antipsychotic medication and 10 age, gender, education, and performance matched healthy comparison subjects underwent fMRI while performing an IL task. On the basis of whole-brain and striatal region-of-interest analyses, we found a relative lack of striatal activation in schizophrenia patients. This result is consistent with convergent evidence of striatal dysfunction in schizophrenia.

The First Joke: Exploring the Evolutionary Origins of Humor

Humor is a complex cognitive function which often leads to laughter. Contemporary humor theorists have begun to formulate hypotheses outlining the possible innate cognitive structures underlying humor. Humors conspicuous presence in the behavioral repertoire of humankind invites adaptive explanations. This article explores the possible adaptive features of humor and ponders its evolutionary path through hominid history. Current humor theories and previous evolutionary ideas on humor are reviewed. In addition, scientific fields germane to the evolutionary study of humor are examined: animal models, genetics, childrens humor, humor in pathological conditions, neurobiology, humor in traditional societies and cognitive archeology. Candidate selection pressures and associated evolutionary mechanisms are considered. The authors conclude that several evolutionary-related topics such as the origins of language, cognition underlying spiritual feelings, hominid group size, and primate teasing could have special relevance to the origins of humor.

Evolutionary Perspectives on Schizophrenia

The theory of evolution may be relevant to psychiatric disorders. Evolution reflects changes in genes throughout time. Thus, evolutionary forces can shape any phenotype that is genetically rooted and that possesses a long history. Schizophrenia is likely an ancient condition with a substantial genetic component. Since the 1960s, several researchers have applied evolutionary principles to the study of schizophrenia. In general, schizophrenia is either viewed as an evolutionary advantageous condition or as a disadvantageous byproduct of normal brain evolution. This paper reviews major evolutionary explanations— historical and current—that speculate on the possible origins of schizophrenia.

Diminished humour perception in schizophrenia: relationship to social and cognitive functioning.

This study attempted to confirm that humour recognition deficits previously found in schizophrenia are specific to the condition and not attributable to other parameters such as depression or anxiety. Secondarily, we explored any possible cognitive or social functioning correlates to humour recognition deficits. A total of 60 participants (20 outpatients with schizophrenia, 20 psychiatric control participants and 20 control participants) underwent a 64-question humour task in addition to a battery of standard cognitive tests and Social Functioning Scales. In order to compare the three groups of participants, we conducted an analysis of variance (ANOVA) and post-hoc t-tests on neuropsychological measures, social functioning measures, and the primary outcome, humour recognition. The schizophrenia group showed significant and substantial deficits in humour recognition compared to the healthy control group, t(38)=5.1, P<0.001, ES=-1.55 and the psychiatric control group, t(38)=3.6, P=0.001. In the schizophrenia group, humour recognition correlated positively with general intellectual functioning (NART) r=.45, P=0.04, social reasoning (WAIS-III Comprehension) r=.54, P=0.01, executive functioning (WCST-CC) r=.69, P=0.001 and social adjustment ratings (SASS scores), r=.54, P=0.02. These findings support the assertion that humour recognition deficits in schizophrenia are specific to the condition and not attributable to other factors such as depression or anxiety. Furthermore, humour recognition deficits in schizophrenia may perhaps be preferentially associated with deficiencies in set shifting and semantic cognition.

Humor perception deficits in schizophrenia

Humor is a complex cognitive process that could be used to elucidate subtle cognitive deficits. Significant deficits in humor perception were observed among 23 outpatients with schizophrenia compared with 20 controls matched for age, gender and education, using a 128-item humor test.

The neural basis of humour comprehension and humour appreciation: The roles of the temporoparietal junction and superior frontal gyrus

Psychological well-being and social acumen benefit from the recognition of humourous intent and its enjoyment. The enjoyment of humour requires recognition, but humour recognition is not necessarily accompanied by humour enjoyment. Humour recognition is crucial during social interactions, while the associated enjoyment is less critical. Few neuroimaging studies have explicitly differentiated between the neural foundations of humour comprehension and humour appreciation. Among such studies, design limitations have obscured the specification of neural correlates to humour comprehension or appreciation. We implemented a trichotomous response option to address these design limitations. Twenty-four participants rated 120 comics (90 unaltered with humourous intent and 30 caption-altered without humourous intent) as either funny jokes (FJ), not funny jokes but intended to be funny (NFJ), or not intended to be funny or non-jokes (NJ). We defined humour comprehension by NFJ minus NJ and humour appreciation by FJ minus NFJ. We measured localized blood oxygen level dependent (BOLD) neural responses with a 3T MRI scanner. We tested for BOLD responses in humour comprehension brain regions of interest (ROIs), humour appreciation ROIs, and across the whole-brain. We found significant NFJ-NJ BOLD responses in our humour comprehension ROIs and significant FJ-NFJ BOLD responses in select humour appreciation ROIs. One key finding is that comprehension accuracy levels correlated with humour-comprehension responses in the left temporo-parietal junction (TPJ). This finding represents a novel and precise neural linkage to humour comprehension. A second key finding is that the superior frontal gyrus (SFG) was uniquely associated with humour-appreciation. The SFG response suggests that complex cognitive processing underlies humour appreciation and that current models of humour appreciation be revised. Finally, our research design provides an operational distinction between humour comprehension and appreciation and a sensitive measure of individual differences in humour comprehension accuracy.

Life History Theory's Best Chance: Illuminating Cluster B Personality Disorders

It was a pleasure to read Marco Del Giudice’s (this issue) target article introducing an evolutionary life history framework for psychopathology. We agree that life history strategies are a likely factor in certain types of abnormal behaviors. There are certainly instances in nature that suggest that organisms vary in the way they allocate their time and resources in the service of optimizing reproductive strategies. In hominids, such disparate reproductive strategies could conceivably lead to changes in behaviors and unique enduring (personality) features. It is an especially compelling idea because variation in reproductive strategies has a long phylogenetic history, and therefore may have fundamentally affected the design of the mammalian neurobehavioral system. Because life history theory has been an understudied concept in the field of psychopathology, Del Giudice’s target article is particularly welcome. Our main critique of the theory is that it is perhaps overreaching and may not apply to every type of psychopathology. We would caution one basic premise in the target article, that is, the supposition that the field of evolutionary psychopathology (i.e., evolutionary psychiatry) is fragmented and requires a unifying principle. Similar to machines, organisms can break down in a variety of unrelated ways (Nesse, 2005). Whether an automobile is disabled by a flat tire or dirty spark plug requires no special theory to connect each type of failure. Similarly, there are many unrelated forms of renal disease (and their only tangible link is that they simply occur in the same organ). Renal dysfunction can be manifested by such disparate conditions as, for example, renal cell carcinoma, polycystic disease, and postinfectious glomerulonephritis. There is no compelling reason to search for a unifying theory to explain these varied kidney ailments. Similarly, the search for a unifying principle of psychopathology may be equally fruitless. Another potential hitch is the possible misapplication of life history principles to modern psychiatric conditions—ailments that have no substantive evolutionary history. Eating disorders are perhaps one of the clearest examples. To our knowledge, the epidemic of classic eating disorders is mostly a modern Western phenomenon; such conditions do not appear to be associated with hunting-and-gathering societies. Therefore, the application of an evolutionary psychopathological theory to an eating disorder—a modern behavioral artifact—may be misplaced. Evolutionary forces will have certainly shaped the underlying neurocircuitry involved in the process of eating behaviors. However, such forces would not have shaped the actual behavioral features of an eating disorder. Instead, eating disorders are probably an accidental by-product of contemporary social problems interacting with the normal neurocircuits that support natural eating behaviors. This is a general criticism that we have toward many evolutionary theories of psychopathology— there is frequently a failure to investigate the deviant behavior inside hunting-and-gathering societies. In our own research, we have always explored the evidence for each psychiatric ailment inside huntingand-gathering societies, and we acknowledge that such evidence is often scant and inconclusive. However, our view is that some perfunctory attempt should always be made to establish the possible phylogenetic history of every psychiatric condition. We also believe that life history theory is dubiously applied to schizophrenia, obsessive-compulsive disorder (OCD) and several subtypes of depression. For example, to tie life history theory to schizophrenia, Del Giudice (this issue) claims that “environmental insults” and “accumulated deleterious mutations” form the basis of schizophrenia (p. 276). However, we believe these are only secondary factors in the development of the condition. Instead, the preponderance of evidence shows that schizophrenia is a highly heritable condition, approaching 85% heritability in some calculations (Cardno et al., 1999). Moreover, the major candidate genes of schizophrenia are neither uncommon nor especially sinister (DTNBP1 [dysbindin], NRG1 [neuregulin 1], COMT, DISC1, RELN; Harrison & Weinberger, 2005). Research articles dealing with hypothesized schizophrenia genes often banter pathological terms (i.e., deleterious mutations), but this is simply because pathological genes are felt to exist and not due to any conclusive evidence.