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Human evolution and the brain representation of semantic knowledge: is there a role for sex differences?

Marcella Laiaconaa, Riccardo Barbarottob, Erminio Capitanic

1. Introduction

2. Clinical and experimental data on patients and normal subjects

2.1. Patients with a disproportionate deficit of plant knowledge

2.2. Patients with a disproportionate deficit of animals knowledge

2.3. General comments on patients' data

2.4. Sex-by-category interaction in normal subjects with reference to animal and plant categories

3. Discussion

3.1. Does familiarity explain everything?

3.2. Can neuropathology explain why males are more defective with fruits and vegetables?

3.3. Are sex differences in processing plant life items supported by neuroanatomical data?

3.4. A reappraisal of familiarity in evolutionary terms

Acknowledgment

References

Copyright

1. Introduction

How semantic knowledge is represented in the human brain and in our cognitive system is one of the most intriguing and debated topics of contemporary neuropsychology. Semantic memory is generally assessed with naming and verbal comprehension tasks, with object-reality decision tasks, and with contrasting semantic probes. Clinical evidence suggests that stored knowledge about objects can be selectively disrupted. Some categories (e.g., biological entities) can be affected such that the meaning of common items is lost, whereas for other categories (e.g., artifacts) stored knowledge can, in the same patient, be almost completely spared (Capitani et al., 2003, Humphreys & Forde, 2001). The most frequently reported type of dissociation is a selective or disproportionate impairment of semantic knowledge about biological categories and a relative sparing of knowledge of man-made objects. There are also cases of semantic category impairments limited to a subset of biological items, such as animals (Caramazza & Shelton, 1998) or plants (Hart et al., 1985).

Several hypotheses have been suggested to explain the origin of semantic category dissociations. One of these, the “Domain Specific Hypothesis” (Caramazza & Mahon, 2003, Caramazza & Shelton, 1998, Mahon & Caramazza, 2003), is evaluated here. Its central assumption is that natural selection has produced specialized, and hence dissociable, neural circuits dedicated to efficient processing of different categories of objects for which rapid identification conveyed reproductive advantages. Knowledge of individual categories is supposedly stored in a brain system downstream from sensory–motor processing. The Domain Specific Hypothesis potentially explains (a) the fact that, typically, all the facets of semantic knowledge (notably, perceptual and functional aspects of the same concept) are evenly impaired or spared in the categories at issue, and (b) the coherence of the observed impairments (animals, plants, conspecifics, and perhaps tools). The evolutionary relevance of these categories is self-evident: animals are potential predators and prey, whereas fruits and vegetables are a source of food and medicine. Nonhuman primates seem to reason differently about three broad domains of objects (animate objects, artifacts, and foods) that correspond to the domain-specific distinctions observed in cases of category-specific impairments (Santos & Caramazza, 2002).

Disproportionate impairment of knowledge of biological items is more frequently reported in males (Capitani et al., 2003). The data concern Alzheimer patients (Laiacona, Barbarotto, & Capitani, 1998), aphasic patients (Laiacona, Luzzatti, Zonca, Guarnaschelli, & Capitani, 2001), and an unselected series of patients affected by herpetic encephalitis (Barbarotto, Capitani, & Laiacona, 1996). Converging evidence comes from studies of single cases selected because they present a given pattern of cognitive deficit. A recent exhaustive review (Capitani et al., 2003) reports details of patients affected by reliable semantic category dissociations described up to 2001: of 61 cases of selective impairment of biological categories, 43 (70.5%) were male. Among the 15 cases presenting the opposite type of dissociation (artifacts more impaired), 8 (53%) were male. These data might suggest that males are more subject to the causes (traumatic brain injury and some types of stroke) of biological-category impairment. However, restricting the analysis to cases with a sex-neutral etiology (herpetic encephalitis) yields a similar result: 21 (75%) of 28 subjects with selective biological impairments were male (Capitani et al., 2003).

Evolutionary accounts of sex differences focus on selection pressures that might have impacted men and women differently. Possibly relevant to the Domain Specific Hypothesis is Silverman and Eals (1992) division-of-labor model. In this view, long-standing foraging specializations, where women gathered plant foods and men hunted animals, have produced a variety of sexually dimorphic cognitive specializations (Gaulin et al., 2005, McBurney et al., 1997, Silverman et al., 2000). Consistent with these accounts, selection may have provided females with more efficient cognitive representation of their main foraging targets, i.e., herbs, fruits, and vegetables.

On this basis, we asked whether the reported male preponderance among patients with selective biological deficits is due merely to the fact that plant stimuli were often used together with animal stimuli in semantic memory batteries. To answer this question, we would need for each case (a) separate reports of performance with animals and plants, based on comparable stimuli, and (b) a statistical comparison between each biological category and man-made objects. These data are not available because the batteries used in different studies included different proportions of animal and plant items, and sometimes lacked fruits and vegetables. However, the answer may be sought with a different approach: the analysis of cases of restricted semantic deficit affecting only animals or only plants, and an examination of data from normal subjects. The hypothesis of a selectively weaker representation of plants in males would be supported if a female superiority with fruits and vegetables, but not with animals, were also observed in normal subjects, and if selective deficits for plants, but not animals, were more common in males. These two questions are treated in turn followed by a discussion of possible causes.

2. Clinical and experimental data on patients and normal subjects

2.1. Patients with a disproportionate deficit of plant knowledge

The findings with these patients are summarized in Table 1.

Table 1.

Cases affected by selective or disproportionate impairment of plant life knowledge

EA (Laiacona, Barbarotto, & Capitani, 2005) Male Herpetic encephalitis/left T (anterior and middle), and minimal right T
ELM (Arguin, Bub, & Dudek, 1996) Male Stroke/bilateral medial T
FAV (Crutch & Warrington, 2003) Male Stroke of left PCA/left T and O
GR (Laiacona, Barbarotto, & Capitani, 1993) Male Head injury/left F–T
JV (Pietrini, Nertempi, Vaglia, Revello, Pinna, & Ferro-Milone, 1988) Male Herpetic encephalitis/left: anterior and medial T, basal F, insula; right: insula
KQu (Goldenberg, 1992) Male Stroke of left PCA/left T and O
MD (Hart, Berndt, & Caramazza, 1985) Male Stroke/left F and basal ganglia
MO (Cornil & Pillon, 2003) Male DAT/cortical and subcortical atrophy (no specific area implicated)
RS (Samson & Pillon, 2003) Male Stroke of left PCA/left T and O
SRB (Forde, Francis, Riddoch, Rumiati, & Humphreys, 1997) Male Artero-venous malformation/left: inferior-medial T, O; right: thalamus
TU (Farah & Wallace, 1992) Male Artero-venous malformation/left O

We report sex, etiology, and lesion site.

F, frontal; T, temporal; O, occipital; PCA, posterior cerebral artery; DAT, dementia of Alzheimer type.

Case EA (Laiacona, Barbarotto, & Capitani, 2005) was initially affected by a global semantic deficit of biological categories as a consequence of herpetic encephalitis. After 10 years, his deficit became minimal for animals, while it remained severe for fruits and vegetables without any further change. The discrepancy between animals and plants was statistically significant at word–picture matching and verbal probes where nuisance variables and difficulty were controlled for.

Case ELM (Arguin, Bub, & Dudek, 1996) was referred to as a category-specific visual agnosic patient. The authors conclude that he was more defective with fruits and vegetables than with animals on picture naming.

Case FAV (Crutch & Warrington, 2003), besides a global anomia, developed a severe difficulty with fruits and vegetables on naming and comprehension tasks and on tests probing semantic knowledge. Word frequency and familiarity were controlled for, and some comparative subjects were selected to control task difficulty.

For case GR (Laiacona, Barbarotto, & Capitani, 1993), the data suggest a greater sparing of animals compared with fruits and vegetables in word–picture matching and on semantic probes.

Case JV (Pietrini, Nertempi, Vaglia, Revello, Pinna, & Ferro-Milone, 1988) presented an overall deficit for natural categories naming and verbal comprehension, and the authors claimed that he was more severely impaired for plants than for animals.

Case KQu (Goldenberg, 1992), on neuropsychological investigations, named fruits and vegetables consistently worse than any other category examined (including animals) both from line drawing and from description.

Case MD (Hart et al., 1985) was impaired with the naming of fruit and vegetable pictures; moreover, he was hesitant when asked to give judgments about the properties of a fruit.

Case MO (Cornil & Pillon, 2003) suffered from a probable dementia of the Alzheimer type. At the beginning of his cognitive deterioration, he was impaired on naming and on word–picture verification with plants. Later (second and third assessment within 18 months), his impairment extended to manufactured objects, but animals were always spared. Stimuli were closely matched for word frequency and sex-specific concept familiarity, but no further data nor any structured statistical analysis was given in the published report. (Thanks to a courteous communication by the authors, we may report further unpublished data on this case.) The plant deficit of MO was certainly of a semantic nature and was also evident in other tasks based on tightly controlled material, e.g., a property-verification task and a naming-to-definition task. Interestingly, MO's deficit was homogeneous for different plant subcategories (fruits, vegetables, flowers, etc.), whereas the patient was neither affected by deficits of color perception nor by a deficit of color knowledge and on categorization tasks he was confused only with fruit and vegetable pictures.

Case RS (Samson & Pillon, 2003) showed a disproportionate naming and conceptual impairment for fruits and vegetables; animals were at intermediate level. Statistical comparisons were carried out taking into account nuisance variables. Neither sex specific familiarity nor a loss of object-color knowledge was at the origin of his fruit and vegetable impairment. He was flawless on object-decision task.

Forde, Francis, Riddoch, Rumiati, and Humphreys, 1997 described case SRB who showed a deficit for natural categories and was more severely impaired on naming of fruits and vegetables than of animals (both on picture naming and on naming to definition), consistent across different tasks.

For case TU (Farah & Wallace, 1992), the authors envisaged a selective naming deficit for fruits and vegetables.

2.2. Patients with a disproportionate deficit of animals knowledge

Deficits limited to the category of animals are exceptional in the literature (Table 2): only three such cases have been described.

Table 2.

Cases affected by selective or disproportionate impairment of animals knowledge

EW (Caramazza & Shelton, 1998) Female Stroke/left F and basal ganglia
LA (Gainotti & Silveri, 1996, Silveri & Gainotti, 1988) Female Herpetic encephalitis/bilateral inferior T, more severe on the left
LH (Farah et al., 1989, Farah et al., 1996) Male Head injury/right T and F, left subcortical O–T, bilateral P–O

We report sex, etiology, and lesion site.

F, frontal; T, temporal; O, occipital; P, parietal.

Case EW (Caramazza & Shelton, 1998) presented very strong evidence of a selective animal deficit. Two other cases, LH (Farah et al., 1989, Farah et al., 1996) and LA (Gainotti & Silveri, 1996, Silveri & Gainotti, 1988), will be included, although the reports were not totally exhaustive.

2.3. General comments on patients' data

The frequencies are small, but we find 11 of 11 males in Table 1 and 1 of 3 males in Table 2: the comparison via Fisher's exact test was significant (p=.033). This evidence suggests that males are more likely than females to present a deficit for plant categories, but not for animals. As such, it seems conservative to suggest that the prevalence of males among patients with a deficit of biological categories (not better distinguished) may depend on the frequent presence of plant stimuli in the test batteries. Regardless, the apparent male vulnerability with the category of plants (or a female advantage for the same category) calls for interpretation.

2.4. Sex-by-category interaction in normal subjects with reference to animal and plant categories

A variety of tasks have been used to study differential semantic knowledge among normal subjects. Picture naming studies examine a fixed and predetermined restricted vocabulary. Semantic fluency tasks examine an unrestricted vocabulary for a specific category in a restricted time span (typically 1 min) and are sensitive to differences among categories in actual vocabulary size. Object-reality decision is a visual perceptual task without verbal components: subjects are asked to judge whether pictures represent real or unreal things. The literature suggests that tasks using plant stimuli are performed better by females, although the same outcome was not observed with animals. A sex difference has been observed by several authors on different tasks (Table 3).

Table 3.

Semantic category dissociations among biological categories reported for groups of normal subjects

Task Semantic categories investigated and sex asymmetry Reference
Picture naming Female superiority for fruits and vegetables. Male superiority for animals McKenna and Parry, (1994)
Picture naming latencies Females faster for natural categories (fruits, vegetables, and animals not analysed separately) Laws (1999)
Semantic fluency Female superiority for fruits and vegetables. No difference for animals Capitani, Laiacona, and Barbarotto (1999)
Semantic fluency Female advantage for fruits but not for animals Laws (2003)
Picture reality decision Female superiority for fruits and vegetables. No difference for animals Barbarotto, Laiacona, Macchi, and Capitani (2002)

Differential familiarity may be a confound. Albanese, Capitani, Barbarotto, and Laiacona (2000) asked a large sample of normal subjects to rate their familiarity with common objects belonging to six semantic categories. Different aspects of familiarity were assessed, but females consistently gave higher familiarity ratings to fruits, vegetables, and furniture items, whereas males showed more familiarity with tools. No sex discrepancies were observed for animals.

3. Discussion

The literature indicates that (a) among brain-damaged subjects, males are more likely than females to present a deficit of the plant category; in fact, no female patients presenting this pattern have been reported to date; (b) the same asymmetry is not documented for the category of animals; (c) the observed male prevalence among deficits for the whole biological realm may stem from the presence of plant stimuli in the batteries used; (d) data from normal subjects indicate a female advantage with fruits and vegetables on a variety of tasks; (e) a study on normal subjects suggests that fruits and vegetable items are more familiar to females than males. On this basis, one might conclude that a higher basic familiarity with the category of fruits and vegetables gives an advantage to females when these categories are investigated in normal subjects and protects the cognitive representation of the same categories in the case of brain damage. However, there are reasons to doubt this superficially appealing explanation.

3.1. Does familiarity explain everything?

A closer look at the clinical data casts doubt on the possibility that familiarity plays a decisive role. Consider case EA (Laiacona et al., 2005, Laiacona et al., 1997). EA, 10 years after HSE, had recovered with animals but not with plants, and at the last examination a selective impairment of fruits and vegetables was evident. The authors used stimuli controlled for male-specific familiarity (Albanese et al., 2000); the latter values were used as a covariate in the analysis of word–picture matching and semantic probe questions, but a significant difference between plants and animals remained. Table 4 reports the mean scores of EA on a task of “pointing to picture on verbal command” and on semantic probes (a totally verbal task) regarding animals, fruits, and vegetables, and also reports the male familiarity with the items employed. EA's better performance with animal stimuli cannot be traced to any familiarity advantage as they were the least familiar items. EA did not have any special premorbid familiarity with animals. After his disease, he retired from work and helped his family, including shopping at the greengrocer, so that he was still in contact with plant objects. However, at the greengrocer, he used a written list prepared by relatives and chose from the shelf the objects whose names matched the words written on the list.

Table 4.

Findings with case EA

Category Mean male familiarity Word–picture matching Semantic probes (n=60)
Artifacts (n=30) 2.36 (S.D.=0.74) 93% (normal >83%) 98% (normal >94%)
Animals (n=10) 1.44 (S.D.=0.24) 100% (normal >70%) 75% (normal >85%)
Fruits+vegetables (n=20) 2.20 (S.D.=0.41) 35% (normal >90%) 52% (normal >91%)

Hits are reported for each task. Semantic probes were six for each stimulus. Familiarity of the stimuli was rated on a 1-to-5 scale (5=very familiar) by 105 males (Albanese et al., 2000). Artifacts included 30 stimuli (10 tools, 10 vehicles, and 10 pieces of furniture), and there were 10 fruit and 10 vegetable stimuli.

A warning against explanations based on familiarity was also given by Samson and Pillon (2003) in their discussion of case RS. Also in this case, the difference between plants and animals was confirmed using sex-specific familiarity values and using fruit and vegetable stimuli that presented the highest familiarity and the lowest visual complexity within the battery. Interestingly, RS's naming of fruits and vegetables contrasted with his naming of domestic implements, a nonliving set likely to match fruits and vegetables for idiosyncratic familiarity since SR stated that he was poorly acquainted with household activities. The patient was impaired with fruits and vegetables but not with domestic implements.

On the basis of the analysis of these two cases, the naïve explanation that males are more impaired with fruits and vegetables because they are not acquainted with shopping at the greengrocers or with cooking seems rather unconvincing. We can also add that a greater premorbid familiarity with a given category seems insufficient to prevent a category from being severely affected by semantic disorders. For instance, case Michelangelo (Sartori, Job, & Coltheart, 1993), who was affected by a severe disorder of the semantic knowledge of animals (not in Table 3 because he was not tested for semantic knowledge of plants), had been an active member of the World Wildlife Fund, and in his premorbid life was acquainted with a vast number of animals. Another case anecdotally cited by Humphreys and Forde (2001) is that of a food expert and wine connoisseur who nevertheless presented a deficit in naming fruits and vegetables after brain damage. Recently, Humphreys and Riddoch (2003) reported a patient (GA) suffering from herpetic encephalitis who, besides an impairment with living categories, also presented a semantic deficit for musical instruments, notwithstanding the fact that he was a former professional musician. As these reports cast doubt on the familiarity account, we should consider alternative explanations.

3.2. Can neuropathology explain why males are more defective with fruits and vegetables?

If we neglect the category-by-sex interaction observed in studies of normal subjects, an explanation could be sought on purely neuropathological grounds. We could reproduce the observed sex by category interaction if the disproportionate deficit of fruits and vegetables were strongly linked to a given lesion site, and if diseases damaging this site were more frequent among male patients. This account is suggested by the evidence that three cases (FAV, KQu, and RS) of plant life impairment (Table 1) suffered from posterior cerebral artery (PCA) stroke that caused unilateral left posterior temporal and occipital damage. However, only three cases out of 11 were affected by PCA strokes. Among the remaining cases, as reported in Table 1, the lesion site did not invariably coincide with the areas supplied by the PCA.

3.3. Are sex differences in processing plant life items supported by neuroanatomical data?

Neuropathological explanations based on a different lesion site between males and females cannot explain why normal subjects show the same sex effect, with a female advantage for fruit and vegetable stimuli. Moreover, the anatomical basis of category specificity is still debated (Martin & Caramazza, 2003). Some biological objects (faces, animals, and plants) typically show peak activity in the lateral portion of the fusiform gyrus; however, the available functional imaging studies do not indicate whether the cognitive representation of animals and plant life is the same or different, and have not investigated whether the hypothetical substrate of these representations coincides in males and females. Therefore, presently, it seems wise to discuss this topic at the level of the behavioral pattern observed in clinical studies rather than at the underlying structural level.

3.4. A reappraisal of familiarity in evolutionary terms

A naïve familiarity account would suggest that acquired cognitive representations of plant exemplars are more robust among females because in their lifetime they have accumulated greater experience with these items. In turn, this implies that the different social roles of males and females may so strongly influence our cognitive system as to create a clinical discrepancy in the frequency of particular neuropsychological disorders, as well as produce parallel effects detectable among normal subjects. But this differential familiarity may have considerable evolutionary time depth (Silverman & Eals, 1992, Zihlman, 1981) and thus may have exerted evolutionary as well as ontogenetic effects on cognitive processes. Females may have specialized on plant resources (and males on animal resources) for many hundreds of thousands of years. But while the evolutionary account can explain the female advantage for plant knowledge, it does not necessarily imply a complementary female deficit for animal knowledge. Humans' interactions with animals may have been as predators or as prey. The latter are clearly relevant to fitness and probably impacted both sexes, and may have overshadowed any pressures arising out of male hunting activity.

The hypothesis that the female advantage for cognitive representation of plants has an evolutionary origin was introduced by Barbarotto, Laiacona, Macchi, and Capitani (2002) and was reappraised by Laws (2003). This account is consistent with a wider theoretical framework able to interpret data from different fields, e.g., female advantage on memory tasks (Gaulin et al., 2005, McBurney et al., 1997, Silverman & Eals, 1992) where familiarity is unlikely to play a role. At a broader methodological level, the possible associations between pathological conditions and normal patterns of performance offer a useful approach to the study of evolved cognitive competencies and the mechanisms that support them.

Acknowledgments

We wish to thank Professor Steven Gaulin for his suggestions and for his criticism on an earlier version of this paper. We are very grateful to Professor Agnesa Pillon for the kind communication of unpublished data concerning the patient MO. Rosemary Allpress revised the English text. This project was partly supported by MIUR grants to EC.

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a Centro Medico di Veruno, “S. Maugeri” Foundation, IRCCS, Neuropsychology Unit, Division of Neurology, Rehabilitation Institute of Veruno, Veruno, Novara, Italy

b Neuropsychology Unit, Istituto “Villa S. Ambrogio,” Fatebenefratelli, Cernusco s/N, Milan, Italy

c Clinic for Nervous Diseases, Milan University, Milan, Italy

Corresponding author. Centro Medico di Veruno, Fondazione S. Maugeri, Via per Revislate 13, 28010 Veruno (NO), Italy. Tel.: +39 0322 884703; fax: +39 0322 830294.

PII: S1090-5138(05)00074-7

doi:10.1016/j.evolhumbehav.2005.08.002



2007:12:08