Edited by: Oscar Arias-Carrión, Hospital General Dr. Manuel Gea González, Mexico
Reviewed by: Graziella Madeo, University of Rome Tor Vergata, Italy; Silmar Teixeira, Federal University of Piauí, Brazil
†Laura Jane Williams and John S. Butler have contributed equally to this work.
Specialty section: This article was submitted to Movement Disorders, a section of the journal Frontiers in Neurology
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The temporal discrimination threshold (TDT) is the shortest time interval at which two sensory stimuli presented sequentially are detected as asynchronous by the observer. TDTs are known to increase with age. Having previously observed shorter thresholds in young women than in men, in this work we sought to systematically examine the effect of sex and age on temporal discrimination. The aims of this study were to examine, in a large group of men and women aged 20–65 years, the distribution of TDTs with an analysis of the individual participant’s responses, assessing the “point of subjective equality” and the “just noticeable difference” (JND). These respectively assess sensitivity and accuracy of an individual’s response. In 175 participants (88 women) aged 20–65 years, temporal discrimination was faster in women than in men under the age of 40 years by a mean of approximately 13 ms. However, age-related decline in temporal discrimination was three times faster in women so that, in the age group of 40–65 years, the female superiority was reversed. The point of subjective equality showed a similar advantage in younger women and more marked age-related decline in women than men, as the TDT. JND values declined equally in both sexes, showing no sexual dimorphism. This observed sexual dimorphism in temporal discrimination is important for both (a) future clinical research assessing disordered mid-brain covert attention in basal-ganglia disorders, and (b) understanding the biology of this sexual dimorphism which may be genetic or hormonal.
The temporal discrimination threshold (TDT) is the shortest time interval at which two sensory stimuli (visual, tactile, or auditory) presented sequentially are perceived as asynchronous by the observer. TDTs increase with age, being a mean of 25–30 ms <35 years of age and 35–40 ms in the 36–65 years age group (
Covert orienting of attention involves the “bottom-up” processing of a salient stimulus. This involves a largely involuntary attentional shift under exogenous control. Particularly salient are abrupt onset stimuli or rapid looming environmental changes. The superior colliculus (SC) and its projections, involved in multisensory detection and integration, have been implicated as key pathways in the generation of covert attentional shifts (
During a temporal discrimination task, visual stimuli reach the wide-field sensory neurons of the SC by the extra-geniculate, retino-tectal pathway (
In a large cohort of healthy participants, we observed age-related effects on the normal TDT; we also noted that women were faster in detecting stimulus asynchrony with significantly lower TDTs than men (
About 175 healthy participants between the ages of 20 and 65 years (88 women, mean age 41.4 years; 87 men, mean age 40.5 years) were recruited from hospital staff and visitors to the hospital. A proportion of participants were recruited for a previous study (
Visual and tactile TDT testing was carried out in a single session in a sound-proof, darkened room, as described previously (
The data were fitted to a cumulative Gaussian function (Figure
Ethics approval for this project was obtained from the Ethics and Medical Research Committee, St. Vincent’s University Hospital. Written informed consent was obtained from all participants.
To investigate the effect of age and sex on the TDT, regression analyses were performed. The combined TDTs for men and for women were submitted to regression analyses with age as the continuous variable. The
Data from all 175 participants, arranged by age and gender group for the mean TDT (in ms), mean PSE (ms), and mean JND (ms), are presented in Table
Age group | 20–30 years | 31–40 years | 41–50 years | 51–65 years | ||||
---|---|---|---|---|---|---|---|---|
Sex ( |
Women (20) | Men (20) | Women (23) | Men (27) | Women (17) | Men (17) | Women (28) | Men (23) |
Mean age in years (SD) | 25.2 (2.5) | 25.6 (2.4) | 34.3 (3.3) | 35.8 (2.9) | 44.9 (3.5) | 43.5 (2.9) | 56.5 (4.3) | 56.9 (5.1) |
Mean TDT in milliseconds (SD) | 43.6 (20.2) | 48.9 (16.3) | 42.9 (17.8) | 55.0 (23.9) | 60.8 (26.5) | 58.2 (17.4) | 70.8 (29.1) | 60.9 (19.5) |
Mean PSE | 29.5 (12.2) | 34.8 (14.9) | 23.6 (17.4) | 36.9 (16.1) | 41.7 (20.5) | 38.6 (12.2) | 41.5 (20.2) | 37.0 (16.2) |
Mean JND | 11.72 (7.3) | 12.8 (4.8) | 15.1 (8.1) | 15.0 (7.1) | 16.2 (8.1) | 17.5 (5.9) | 22.1 (11.8) | 17.3 (6.4) |
For women, the analysis revealed that age explained a significant amount of the variance in the TDT values [
For men, we noted a trend toward significance for age explaining the variance in the TDT values [
Thus, influence of age on the mean combined TDT score is such that the TDT worsened by approximately 1 ms per annum in women (Beta = 1.042) and by 1 ms every 3 years in men (Beta = 0.332). The comparison of the fit analysis revealed a significant difference in the intercepts between the groups [
In women, age explained a significant amount of the variance in the PSE values [
For men, there was no significant relationship between age and PSE values [
The comparison of fit analysis revealed a significantly different intercept between the groups [
Age also explained a significant amount of the variance in the JND values in women [
In men, age explained a significant amount of the variance in the JND values [
The comparison of fit analysis revealed no significant difference in the intercepts between the groups [
Women, aged 20–40 years, have faster temporal discrimination than men; 20-year-old women were approximately 13 ms faster than age-matched men, representing a 20% advantage. Under the age of 40 years, women had a lower PSE value than men indicating shorter inter-stimulus intervals at which they were equally likely to detect two stimuli as synchronous or asynchronous. Women in the 20–40 years age-group were also more sensitive to change in stimulus asynchrony around their PSE as demonstrated by lower JND values. Thus, in the 20–40 years age group, women were both more sensitive and more accurate in temporal discrimination than men. Mean TDT scores in women increased (worsened) with age more than in men. Above the age of 40 years, women lose this initial advantage and had longer mean TDTs than their male peers. TDTs in women deteriorated at a rate of about 1 ms/year, while TDTs in men deteriorated at a rate of only 1 ms every 3 years. The PSE was also more influenced by age in women, remaining relatively unchanged in men despite increasing age. However, for both men and women, the JND increased as a function of age. This would suggest that the perception of asynchronous (PSE) stimuli is function of age and sex, while the reliability of the percept (JND) is a function of age but is not significantly different between men and women.
This sexual dimorphism in temporal discrimination raises interesting questions when one considers the underlying mechanisms of temporal discrimination and the pathways involved. We propose that temporal discrimination is a function of the midbrain-basal ganglia network for covert orienting of attention, with lower TDT scores representing more efficient collicular-basal ganglia processing of salient stimuli or environmental change. Numerous studies have identified cognitive, neuroanatomical, and biochemical correlates of attention and have noted sexual dimorphism (
We observed deterioration of temporal discrimination in women with age, significantly more marked than in men, indicating age-related sexual dimorphism in covert attention network function. Is the midbrain-basal ganglia network more sensitive to age in women? In attention tasks with spatial cues, reflexive allocation of attention has been found to be well preserved in older healthy individuals (
Sexual dimorphism in attention strategies may be of evolutionary significance and have implications in terms of survival. Body size dimorphism can dictate sex-specific roles within species such as the need for younger females to protect offspring from predators. Female eastern gray kangaroos are physically smaller than their male counterparts and are noted to display increased vigilance behaviors and scanning for predators compared to males (
Looming stimuli are powerful in engaging covert attention. Detection of looming stimuli with shift in attention and subsequent motor response are vital functions in terms of survival. We activate such processes while playing sport or crossing the road; in other animals, they are essential for prey and predator detection. Responses to looming stimuli are observed in many species: insects, pigeons, rodents, and non-human primates, with key involvement of the optic tectum/collicular pathways. Evidence in humans from neuroimaging studies indicates the SC is activated by multisensory looming stimuli (
It is not yet clear whether the relationship between attention and sex, and its change over time, is mediated by genetic sex, or hormonal factors, or both. Interestingly, sex chromosome genes (independent of their gonadal effects) have been implicated in neurodevelopment and neural function including attention. For example the “Sex-determining region on the Y” gene (
Gender dimorphism has been recorded in many neuroanatomical studies, with functional magnetic resonance imaging (fMRI) revealing increased neural activation in women in areas such as the putamen, thalamus, and midbrain during visual processing (
The SC plays a key role in the generation of covert attention (
Studies have also proposed that GABA is under the influence of genetic sex. X chromosome genes appear to influence enzymes involved in GABA synthesis and levels of GABA neuron markers (
One limitation of our study is that we assume a linear relationship of TDT with age. We have only included individuals from 20 years old up to the age of 65 years. An interesting study in the future would be to examine TDTs in both younger (children) and older individuals. It is not clear whether the observed advantage in women under the age of 40 years is secondary to genetic sex or hormonal influences. To help clarify this, a future study could also examine TDTs in relation to hormonal status and function, including menstrual variation, menarche, and menopause. However, repeated TDT testing of subjects in each menstrual cycle phase may open the experiment to a possible practice effect. The 175 healthy participants ranged in age from 20 to 65 years, and were assessed in relation to medical history and a neurological examination; however, mental state examination was not formally assessed. Subclinical cognitive impairment would, however, be highly unlikely in this cohort, and would have been evident in the reproducibility of responses in the test procedure.
Temporal discrimination has been applied as a mediational endophenotype in AOIFD (
Recognition of sex differences in neural and cognitive function is vital to our understanding of neurological disorders and elucidation of pathology. Our findings add to the body of evidence that women have a superior ability to covertly shift attention. The results raise interesting questions regarding the evolutionary development of the network for covert orienting of attention in a sex- and age-dependent manner. The results also point to sexual dimorphism within the GABAergic system, which warrants further investigation. This could have clear implication for research into neurological disorders, including movement disorders, Alzheimer’s disease, schizophrenia, and autism, where GABA dysfunction has been suggested (
This work emphasizes the importance of considering both age and sex, when interpreting the TDT test and in its application as a meditational endophenotype.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
This study was supported by grants from Dystonia Ireland, the Irish Institute for Clinical Neuroscience, the Foundation for Dystonia Research (Belgium), and the Health Research Board, Ireland, Clinical Scientist Award (CSA-2012/5).