Sex differences in many spatial and verbal tasks appear to reflect an inherent low-level processing bias for movement in males and objects in females. We explored this potential movement/object bias in men and women using a computer task that measured targeting performance and/or color recognition. The targeting task showed a ball moving vertically towards a horizontal line. Before reaching the line, the ball disappeared behind a masking screen, requiring the participant to imagine the movement vector and identify the intersection point. For the color recognition task, the ball briefly changed color before disappearing beneath the mask and participants were required only to identify the color shade. Results showed that targeting accuracy for slow and fast moving balls was significantly better in males compared to females. No sex difference was observed for color shade recognition. We also studied a third, dual attention task comprised of the first two, where the moving ball briefly changed color randomly just before passing beneath the masking screen. When the ball changed color, participants were required only to identify the color shade. If the ball didn't change color, participants estimated the intersection point. Participants in this dual attention condition were first tested with the targeting and color tasks alone and showed results that were similar to the previous groups tested on a single task. However, under the dual attention condition, male accuracy in targeting, as well as color shade recognition, declined significantly compared to their performance when the tasks were tested alone. No significant changes were found in female performance. Finally, reaction times for targeting and color choices in both sexes correlated highly with ball speed, but not accuracy. Overall, these results provide evidence of a sex-related bias in processing objects versus movement, which may reflect sex differences in bottom up versus top-down analytical strategies.

Funding: The work was supported in part by University of California San Diego Academic Senate Grant RJ145G (Pineda). No additional external funding was received for this study. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Introduction

The majority of human cognitive sex differences are broadly categorized as ‘spatial’ or ‘verbal’ [1]. To what degree these differences arise from lower level perceptual processing is unknown, but functional studies of neurophysiological and behavioral sex differences in humans, as well as similarities in cognitive sex differences observed in humans and animals, suggest this possibility [2]. Below we review evidence that the kinds of spatial and verbal skills that show cognitive sex differences may involve differential processing of information involving the dorsal and ventral processing streams that are common to all mammals.

Dorsal and ventral stream cortical processing provide a functional analysis of movement and object recognition, respectively. The dorsal stream provides the basis for conscious and unconscious knowledge of ‘where’ something is in visual space, as well as the tracking of object movement. Ventral stream processing provides information for conscious recognition of ‘what’ something is, including its associated characteristics [3]–[4]. Both cortical streams operate in parallel, with some integration of movement and objects occurring in subdivisions of the dorsal stream that lies anatomically between the two classical pathways [5].

Spatial tasks showing reliable sex differences in men include targeting, maze learning, and dis-embedding tasks such as Rod and Frame and Embedded Figures [6]–[7], all of which involve processing of actual or abstract movement. Some corollaries to these sex differences are observed in animals. For instance, maze learning across species consistently favors males in environments that depend upon employing a cardinal orientation strategy [8]–[10]. Similarly, targeting tasks that involve accuracy in throwing an object also favor males across species [11]–[14]. More complex tasks involving space relations, such as mental rotations, have no direct corollary in animals, but are proposed to partially rely on neural substrates associated with targeting skills [12].

In spite of the categorical label, verbal tasks that show sex differences are not easily related to differences in inherent linguistic ability since men and women exhibit similar writing skills, vocabulary, general fluency, and language and reading comprehension [13]–[14]. Instead, tasks in this category showing sex differences rely on verbal or written expression of knowledge related to objects (or events) and their associated characteristics. These include fluency in naming words beginning with a given letter, autobiographical and episodic memory, and communication skills, all of which favor women [6],[14]. The pattern suggests that females have a broader network of associations among objects than males, which allows for greater verbal elaboration and description. This is consistent with the greater bilateral cortical activation in women, as well greater activation of the left temporal pole, during passive listening to narratives or verbal descriptions related to episodic memory [15]–[16].

More direct evidence of a female advantage related to object processing comes from studies where participants are exposed to incidental visual stimuli and subsequently tested for their recall. Under both real-life and experimental conditions, females exhibit better implicit memory for object recall than males, in addition to showing greater recall of the object location [17]–[19] The unconscious aspect of the female advantage in object recall is emphasized by findings showing that no gender difference is observed when participants know the nature of the task [20]. Interestingly, although object location memory and object identity memory are distinctly different tasks, Voyer et al. observed a .37 Pearson correlation between the two tasks in a sample of 223 participants, suggesting that performance in both may rely on a common mediating process [17]. Choi and L'Hirondelle [21] have proposed that verbal memory may account for the female advantage, which is supported by a number of these kinds of implicit memory studies where no sex difference was observed when the objects were uncommon or not nameable [22]–[24].

The object location memory task favoring females involves a spatial skill [18] [25]–[26] that is distinct from space relation skills inherent to the tasks favoring males such as mental rotation or embedded figures. In the object location task, females are thought to place more reliance on semantic encoding of the object as the primary organizational strategy, with space relations taking a secondary role, whereas males may use space relations as the primary strategy [17] [27]. This kind of sex related pattern can also be observed in studies of navigational strategy. Navigating an environment can be successfully accomplished using either a landmark based strategy or one that relies on cardinal information (East, West, North, South). Both strategies are available to both sexes, but in a choice situation women are more likely to use landmarks, while men are more likely to rely on cardinal orientation [28]–[29]. Similar sex differences in navigational strategy are found in non-human primates and rodents [30]–[32].

Activity within ventral and dorsal streams is innately bound to cognitive development through their inherent capacity to build an associational library linking form and function in the brain [33]–[35]. For this reason, early biological or environmental influences that bias processing in one stream over the other can be expected to induce long-term effects on some aspects of cognition across species. An important biological role for androgens is indicated by numerous studies of sexual differentiation of the brain and behavior [2],[36]–[37]. Animal studies manipulating early androgen exposure have demonstrated that the male advantage in visuospatial skills is the result of a phenotypic influence of early androgen exposure rather than a direct genetic influence on visuospatial brain organization, since females treated briefly with androgens in early development showing male performance levels in adulthood [7]. Evidence to support a similar organizational role for early androgen exposure in humans is found in women with Congenital Adrenal Hyperplasia (CAH). These women are exposed to higher than normal levels of androgens in early development and subsequently perform as well as typically developing men on a number of spatial tasks that rely on the analysis of real or imagined movement, including mental rotations, the Rod and Frame Task, and targeting tasks such as throwing darts or catching a ball [38]–[39].

The content of free drawings of preschool age boys and girls offers additional indirect support for an organizing role of androgens in developing a functional bias toward processing movement [40]. Compared to typically developing girls, the drawings of girls with CAH and typically developing boys are significantly more likely to a) portray moving or mechanical objects, b) depict a three dimensional arrangement, c) use fewer and darker colors, and d) show attempts at portraying objects dynamically with their function. In contrast, the drawings of typically developing girls are more likely to a) show people, b) use more and warmer colors, and c) have objects arranged in a row without regard to realistic/relative size. These findings have a parallel in the results from studies of children's toy preferences. Typically developing boys and girls with CAH prefer toys that move, such as trucks, whereas typically developing girls prefer clothes, household items, and dolls [39]. At first glance these results appear to reflect a strong cultural bias, but this interpretation is tempered by a report of similar sex differences in the preferences for human toys in non-human primates [41].

For many of the tasks that show cognitive sex differences in humans, two performance strategies are available; one that favors a ‘bottom-up’ analysis versus one that relies on top-down analysis. In the bottom-up approach, perceptions emerge from data acquired through sensory input, in contrast to a ‘top down’ approach where perception relies on prior knowledge used to interpret that data. Bottom-up processing in higher cognitive tasks relies on both dorsal and ventral stream analysis, which is subsequently elaborated by top-down frontal analysis [42]. It is the degree to which top-down analysis is involved in the process that determines the bottom-up versus top-down distinction.

During mental rotation tasks, greater activation of bottom up processing within the dorsal stream is consistently observed in males compared to females, while greater activation of frontal circuitry is observed in women [43]–[46]. Interestingly, when activation patterns are compared in men and women with equal performance on mental rotation tasks, the sex difference in bottom-up versus top-down activation still remains [47]–[48]. The pattern suggests that women are more likely to use an analytical, top-down approach that compares and contrasts object features to solve the mental rotation problem, while males are more likely to rely on dorsal stream processing associated with mentally rotating the figures for comparison. A similar pattern of results has been observed for auditory spatial tasks, wherein males show greater bottom-up processing for sound location than females [49].

Based on this overall pattern of sex cognitive sex differences suggesting a bottom-up processing bias for movement in men and a top-down process bias in women, we reasoned that the large gender differences observed in targeting tasks might be reduced or eliminated by changing task requirements to go against the hypothesized bottom up strategy of males. To test this, we developed a computer task that employed a vertically moving ball that could be adapted for targeting or object recognition. Traditionally, ‘targeting’ is a term used to characterize tasks that require estimating the path (or vector) that an object is travelling, or will travel, as reflected in tasks such as throwing darts and catching a baseball. Most targeting studies in the literature that show sex differences involve tasks that include a significant degree of motor coordination as part of the response (e.g., throwing a ball or catching an object), although it is assumed that sex differences in task performance are primarily perceptual [12], [14]. We sought to confirm this by designing the computer task to eliminate an essential reliance on hand-eye motor coordination in the response. We also chose to use a targeting type of task for these experiments because these kinds of tasks show the largest sex differences among cognitive skills, with reported size effects ranging between 1.0 and 2.0 [14]. In addition, targeting skills have a relatively small cognitive load compared to more complex spatial tasks such as mental rotation or embedded figures, but are proposed to play an indirect role in higher-level spatial tasks that rely on abstract movement [12].

We employed three testing conditions in these experiments. The first was a targeting condition, where participants were instructed to estimate where a moving ball would intersect a horizontal line. The ball always disappeared behind a mask before reaching the intersect line. The second condition employed the same stimuli, but examined sex differences in conscious object recognition. Here, a white ball moving toward the horizontal line changed color for 100 milliseconds just before it went beneath the mask. Participants were required to identify the shade of the color to which it changed by choosing among four choices that appeared after the ball crossed the line. No targeting response was required and participants tested in this condition were given no experience with the targeting condition. These two conditions are depicted in Figure 1.

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larger image TIFF original image Download: Figure 1. The four EVITA ball movement perspectives are shown in the top two rows. In the color shade recognition condition (represented in the bottom row), on 50% of the trials a white ball changed randomly to a shade of red, blue or yellow just before it goes under the masking shade. Participants choose the color shade from four choices on the top of the screen. https://doi.org/10.1371/journal.pone.0032238.g001

The third condition was a dual attention condition designed to require participants to prepare for both targeting and color recognition at the start of a trial. In this task, the ball randomly changed color on half of the trials, requiring participants to identify the color shade. On the trials where the ball did not change color, participants estimated the point of intersection. In this dual attention condition, we expected males to experience a degree of interference at the start of each trial because they are holding opposing strategies that depend upon whether it will be a targeting or color recognition tasks. The interference would derive from their bias toward bottom up-processing for targeting, which goes against the required top-down strategy for object recognition. Therefore, we expected male targeting performance to be relatively impaired in this condition compared to performance observed when only targeting was required. In contrast, we reasoned that a top-down strategy for targeting in females should present little interference and their performance should be similar to targeting alone. Support for these hypotheses is provided in the results of the studies described below.