Is it reasonable to expect that latent infection with T. gondii
could have an effect on human behavior and possibly even transcultural differences15
? The studies reviewed suggest that T. gondii
may have subtle effects on personality and psychomotor performance. If so, this would be consistent with the effects of T. gondii
on rodent behavior, as described in the accompanying article by Webster.
In the rodent model, the effects of T. gondii
are best explained in evolutionary terms by the manipulation hypothesis, ie, the parasite changes the behavior of the rodent in such a way as to increase the chances of the parasite's getting into a feline and completing its life cycle. Humans are dead-end hosts for T. gondii
, because the chances that a human being will be eaten by a feline are infinitesimally small. Among our primate ancestors, however, this was not always the case,16
as suggested also by contemporary studies of the frequency with which monkeys and apes are eaten by large felines in Africa. For example, a study performed in the Ivory Coast confirmed that primates account for a large proportion of leopards' diet and revealed the predation pressure exerted by large felines on 8 different monkey and 1 chimpanzee species.17
In addition, parasites are not aware that they have entered dead-end hosts, so they are likely to exert whatever effects they do in any host. In this regard, it is interesting to consider the increase in traffic victims among T. gondii
–infected humans as a contemporary example of manipulation activity of a parasite. It is also possible that the effects of the parasite are not due to the manipulation in an evolutionary sense but merely due to neuropathological or neuroimmunological effects of the parasite's presence.
Alternate explanations for the effects of T. gondii
on humans cannot be ruled out. It is possible, eg, that individuals with certain personality characteristics behave in a manner that makes it more likely that they will become infected. For example, it was found that specific risk factors for Toxoplasma
infection, such as contact with cats and the eating of raw or undercooked meat, were also related to some of Cattell's personality factors. However, these personality factors were different from those related to Toxoplasma
Confounding factors must also be considered as possible explanations. For example, in some countries, infection with T. gondii
occurs more commonly in rural areas that is also where individuals are likely to have less education and consequently score lower on tests of verbal intelligence.18
This can produce a spurious association between T. gondii
infection and intelligence.
If latent T. gondii
infections are exerting effects on human personality characteristics and behavior, what is the possible mechanism? It is known that T. gondii
increases dopamine in rodents19
and also that treating the rodents with a selective dopamine uptake inhibitor differentially alters the behavior of the infected and uninfected rodents.20
Also the observed low level of novelty seeking in humans infected with Toxoplasma
or cytomegalovirus is supposedly associated with high dopamine levels in the ventral midbrain.7,8
The mechanism of the dopamine increase by T. gondii
is not known but may involve the inflammatory release of dopamine by increasing cytokines such as interleukin-2.21,22
The dopamine imbalance between the mesolimbic and mesocortical regions in the brain is suspected to play a role in the development of schizophrenia,23,24
which could explain the observed association between schizophrenia and toxoplasmosis (see related articles in this issue of Schizophrenia Bulletin
It is also possible that differences in the level of testosterone may be responsible for the observed behavioral differences between Toxoplasma
-infected and Toxoplasma
-free subjects. A lower second- to fourth-digit length ratio,25
greater body height in men,25
longer duration of pregnancy,26
and higher sex ratio (ie, more male births)27
suggest that Toxoplasma
-infected subjects have a higher level of testosterone. High levels of steroid hormones have been associated with lower cellular immunity.28,29
Thus, the most parsimonious explanation of the observed high testosterone–toxoplasmosis association is a higher risk of Toxoplasma
infection in subjects with higher levels of testosterone and therefore a weaker immunity. Alternatively, in an evolutionary sense, the behavioral changes induced by T. gondii
could be side effects of the organism's increase in testosterone in order to impair the cellular immunity of the host and thus increase the chances of surviving in the host organism.
The results obtained during the past 15 years strongly suggest that latent toxoplasmosis influences the behavior not only of rodent hosts but also of humans. The neurophysiological mechanisms and practical effects of these behavioral changes, however, are still to be elucidated.