Research reportSex differences in attentional processes in adult rats as measured by performance on the 5-choice serial reaction time task
Highlights
► We examined attentional processing in adult male and female rats. ► Sex differences were revealed under challenging conditions. ► Males displayed greater vigilance than did females. ► Females exhibited greater inhibitory control than did males.
Introduction
Sex differences have been documented throughout the brain using techniques ranging from single-unit recordings to systems level brain imaging [For review, see 1]. In addition, basic behavioral research has generated support for the influence of sex and gonadal hormones on cognitive performance across a variety of tasks [For review, see 2]. In humans, males outperform females on tasks of mental rotation and navigation [3], [4], [5], [6], and females outperform males on tasks of verbal memory [7], [8], [9]. Most behavioral research conducted using nonhuman animal models has focused on sex differences that arise during acquisition and performance of hippocampal dependent tasks [For review, see 2]. For example, male rodents outperform female rodents on tasks of spatial memory, as measured on the radial arm maze and Morris water maze tasks [10], [11], [12], [13], [14], [15]. However, reports indicate that these results can vary with age, stress levels, and task demands [16], [17], [18], [19]. Fewer animal studies have examined possible sex differences in tasks dependent upon other brain areas, including the prefrontal cortex [20], [21], [22], an important brain area for attentional processes [23], [24], [25].
Sex differences in the types of attentional problems displayed in certain neuropsychological disorders, including attention deficit hyperactivity disorder (ADHD) and schizophrenia, suggest that males and females may differ in the way that they process attentional information. For example, decreased vigilance, the ability to continuously allocate attentional resources in order to detect rare events [24], and decreased inhibitory control, the ability to refrain from making a premature or inappropriate response [25], are symptoms of ADHD [26]. The prevalence of ADHD is higher for males than it is for females. Males with ADHD display greater impulsive symptoms, and females with ADHD display greater inattentive symptoms [26], [27]. Poor focus on tasks and excited, uncontrollable motor behavior are symptoms of schizophrenia [28]. The onset of schizophrenia is earlier in males than it is in females [29], and it has been suggested that estrogens may exert a protective effect against schizophrenia [30]. Whether these sex differences seen in pathological states are a function of differences in the general population is unclear.
Investigations of attentional processes using rodent models have typically focused on males [23], [24], [25], [31]. The few studies that have directly compared male and female performance on attentional tasks have found mixed results. Some report a male advantage in vigilance and a female advantage in inhibitory control during attentional processing tasks [20]. Others report no or little effect of sex during attentional processing tasks [21], [22]. The conflicting results of these studies could be due to differences in the demands of the tasks used in the studies or due to the relatively small amount of training before testing. Many sex differences disappear with extended training [2], [18]. This disappearance could be due to differences in acquisition rate, but could also be due to the influence of sex on variables unrelated to task demands, such as anxiety or stress. Assessment of sex differences in attentional processes after extensive training decreases the influence of these variables on performance.
Circulating levels of testosterone and estradiol can affect attentional processing in male and female rats. For example, decreased levels of testosterone following gonadectomy impair the acquisition of an operant extradimensional set shifting task in male rats [32], and estradiol improves vigilance during performance of an attentional processing task in ovariectomized female rats [33]. The effect of testosterone and estradiol on attentional processing indicates that the different levels of gonadal hormones circulating in males and females could contribute to a sex difference in attentional processing.
Sex differences in vigilance and inhibitory control can be assessed using procedures that have been developed to model particular aspects of attention in rodents. The 5-choice serial reaction time task (5-CSRTT) was developed from the continuous performance task used to quantify attentional deficits in humans [24]. In the 5-CSRTT, rats must identify the location of a brief light stimulus presented randomly across five possible locations over a large number of independent trials [31]. The 5-CSRTT has been shown to be dependent upon the prefrontal cortex [24], and assesses both vigilance, the rats ability to sustain attention across the many trials, and inhibitory control, the rats ability to refrain from making a response until the appropriate time. To date, male and female performance on the 5-CSRTT has not been directly compared.
The goal of the current study was to use the 5-CSRTT to examine sex differences in attentional processes in adult rats. Performance was assessed under baseline conditions and under behavioral challenge conditions during which task difficulty was increased. Behavioral challenge conditions included shortening the stimulus duration, shortening the time before the onset of the stimulus, lengthening the time before the onset of the stimulus, and presenting a distracting noise.
Section snippets
Subjects
Fourteen male and fourteen female Long-Evans hooded rats, approximately 2 months of age, were purchased from Harlan Sprague Dawley Inc. (Indianapolis, IN). Animal care was in accordance with the guidelines set by the National Institutes of Health Guide for the Care and Use of Laboratory Animals, and all procedures were approved by the Institutional Animal Care and Use Committee of Tulane University. Animals were individually housed under a 12-h light/dark cycle and tested during the light phase
Results
Four male and five female animals failed to reach criterion level performance during training and were excluded from all analyses, resulting in the following final group numbers: male (n = 10), female (n = 9).
Discussion
The results of the present study reveal sex differences in attentional processes in adult rats under challenging conditions. Adult female rats display less vigilance than do adult male rats during performance of the 5-CSRTT. Conversely, adult male rats exhibit less inhibitory control than do adult female rats. Vigilance, as measured by percent correct and number of omissions, was more disrupted in female rats than it was in male rats during the behavioral challenges. Female rats displayed a
Acknowledgments
This work was supported by the National Science Foundation grant 0951008 to JMD and a State of Louisiana Board of Regents Graduate Fellowship, LEQSF(2009-2014)-GF-13, to DWB.
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