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Different Patterns of Puberty Effect in Neural Oscillation to Negative Stimuli: Sex Differences

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Different Patterns of Puberty Effect in Neural Oscillation to Negative Stimuli: Sex Differences Different patterns of puberty effect in neural oscillation to negative stimuli: sex differences Jiajin Yuan, Enxia Ju, Jiemin Yang, Xuhai Chen & Hong Li Cognitive Neurodynamics ISSN 1871-4080 Volume 8 Number 6 Cogn Neurodyn (2014) 8:517-524 DOI 10.1007/s11571-014-9287-z 1 23 Your article is protected by copyright and all rights are held exclusively by Springer Science +Business Media Dordrecht. This e-offprint is for personal use only and shall not be self- archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Cogn Neurodyn (2014) 8:517–524 DOI 10.1007/s11571-014-9287-z BRIEF COMMUNICATION Different patterns of puberty effect in neural oscillation to negative stimuli: sex differences Jiajin Yuan • Enxia Ju • Jiemin Yang • Xuhai Chen • Hong Li Received: 16 December 2013 / Revised: 4 March 2014 / Accepted: 21 March 2014 / Published online: 28 March 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract The present study investigated the impact of but not in pre-pubertal girls. On the other hand, the size of puberty on sex differences in neural sensitivity to negative the emotion effect for HN stimuli was similar for pre- stimuli. Event-related oscillation technique was used. pubertal boys and girls; while this effect was significantly Because girls are more vulnerable to affective disturbances more pronounced in pubertal girls compared to pubertal than boys during adolescence, it was hypothesized that boys. Additionally, the size of the emotion effect in gamma puberty exerts different influences on neural sensitivity to oscillations decreased as a function of pubertal develop- negative stimuli in boys and girls. EEGs were recorded for ment during both HN and MN stimulation in boys. For highly negative (HN), mildly negative (MN) and neutral girls, the emotion effect in gamma oscillations increased pictures, when boys and girls distinct in pubertal status with pubertal development during HN stimulation. Thus, performed a non-emotional distracting task. No emotion puberty is associated with reduced neural sensitivity in effect and its interaction with sex and puberty were boys but increased sensitivity in girls, in reaction to neg- observed in response latencies. However, puberty influ- ative stimuli. The implications of these results for the enced the gamma-band oscillation effect for negative psychopathology during adolescence were discussed. stimuli differently for boys and girls: Pre-pubertal boys showed a significant emotion effect for HN stimuli, whose Keywords Pubertal transition Á Emotional sensitivity Á size was decreased in pubertal boys. By contrast, there was Sex differences Á Event-related brain oscillations (ERO) a significant emotion effect for HN stimuli in pubertal girls Introduction Many studies indicated a higher prevalence of affective J. Yuan (&) Á J. Yang Key Laboratory of Cognition and Personality of Ministry disturbances in females relative to males during adolescence of Education, School of Psychology, Southwest University, (Patton and Viner 2007; Nolen-Hoeksema 2001; Kessler No. 1 of Tiansheng Road, Beibei, Chongqing 400715, China et al. 1993). The greater prevalence of depression in women e-mail: [email protected]; [email protected] was reported to emerge at early adolescence, approximately E. Ju from 13 years of age and persists until midlife (Angold and Chongqing Preschool Education College, Rutter 1992; Nolen-Hoeksema 2001). In early studies, Wanzhou, Chongqing 404047, China researchers reported that the rates of depression were similar or lower in pre-pubertal girls in comparison with pre- X. Chen Key Laboratory of Behavior and Cognitive Psychology in pubertal boys (Angold and Rutter 1992; Angold et al. 1998; Shaanxi Province, School of Psychology, Shaanxi Normal McGee et al. 1990; Wichstrom 1999), whereas depressive University, Xi’an 710062, China disorders began to be more prevalent in girls versus boys from pubertal transition (Angold and Rutter 1992; Ge et al. H. Li Research Center for Psychological Development and Education, 2006; Kessler et al. 1993). Also, pubertal development Liaoning Normal University, Dalian, Liaoning, China is linked with a greater prevalence of other affective 123 Author's personal copy 518 Cogn Neurodyn (2014) 8:517–524 disturbances in girls compared to boys, such as panic dis- Particularly, pubertal development of boys is associated order, social anxiety disorder and dysthymia (Deardorff et al. with intensified masculine gender identity, a trait that pre- 2007; Hayward et al. 1992; Patton and Viner 2007). disposes boys to be assertive, instrumental and less emotion- Nevertheless, the mechanisms underlying this sex dif- focused (Wichstrom 1999). Thus, it is likely that pubertal ference are unclear. There were a number of studies sug- boys are less reactive to negative stimuli compared to pre- gesting that psychosocial factors, such as the girls’ more pubertal boys. If these hypotheses are confirmed, the sex concerns about body image, might interact with biological differences in the prevalence of affective disturbances dur- factors (e.g. more hormonal fluctuations in girls) to con- ing adolescence may be explained, at least in part, by the tribute to this phenomenon (Hankin and Abramson 2001; girls’ enhanced reactivity and the boys’ decreased reactivity Angold et al. 1999). However, most of these studies relied to negative stimuli during pubertal transition. on questionnaires and psychometric methods, such as In life settings, emotional responses are often triggered treating psychosocial and hormonal measurements as pre- by unpredictable stimuli during non-emotional activities dictors, and depressive symptoms as outcomes (Angold (Delplanque et al. 2005; Yuan et al. 2007). Thus, an et al. 1998, 1999; Hayward et al. 1999; Wichstrom 1999; experimental design that presents emotional stimulus Nolen-Hoeksema and Girgus 1994). Accordingly, the unpredictably and that does not require subjects to assess conclusions were primarily based on regression methods stimulus valence, may allow emotional responses in the (e.g. Angold et al. 1998, 1999; Wichstrom 1999; Nolen- laboratory setting to more closely resemble those in natural Hoeksema and Girgus 1994), and seldom experimental settings (Delplanque et al. 2005). Thus, to increase eco- evidence was available to date that directly examines this logical validity of emotion induction, the present study phenomenon. used a distracting oddball task that required subjects to To better understand why girls become more vulnerable make a standard/deviant distinction by pressing different to affective disturbances than boys during adolescence, it is keys, irrespective of the emotionality of the deviants. necessary to use experimental methods, by which we are Considering that negative stimuli of distinct valence able to manipulate the emotionality of stressful stimuli and strengths often influence cognitive functions differently directly assess how sex and puberty may influence one’s (Yuan et al. 2012), we manipulated negative stimuli into behavioral and physiological reactivity to stressful stimuli. two valence levels: highly or mildly negative. The use of experimental approach is important, because On the other hand, compared to the classic event-related previous studies suggest that individuals with greater sen- potential method that is restricted to low-pass filtering and sitivity to emotionally stressful stimuli, are usually more phase-locked averaging, neural oscillation is able to provide vulnerable to negative emotions and affective disturbances richer information, such as non-phase-locked and fast (Hofer et al. 2006; Gohier et al. 2013). A typical example is rhythmic (e.g. gamma rhythm) indexes of emotion arousal that adult females, a population known for the enhanced (Bastiaansen and Hagoort 2006). Based on this consider- brain sensitivity to negative stimuli (Hofer et al. 2006; ation, we used event-related oscillations (ERO) to investi- Yuan et al. 2009), have a higher prevalence of affective gate the influence of puberty on brain sensitivity to negative disturbances than adult males (Altemus 2006; Simon et al. stimuli and sex differences. Specifically, it has been 2006). Additionally, it is well known that pubertal devel- reported that the power of high-frequency gamma oscilla- opment is a land-marking event of adolescence, which tions in EEGs is sensitive to negative stimulation, and the significantly influences both health and social adaptation gamma power behaves as a valid index of emotion arousal (Patton and Viner 2007). Thus, to understand the girls’ to stressful stimuli (Balconi and Lucchiari 2008; Balconi vulnerability to affective disturbances during adolescence, et al. 2009). Thus, we chose gamma oscillatory activities as it would be helpful to investigate the influence of puberty an index of the emotional arousal effect and its interaction on brain sensitivity to negative stimuli, and how this with puberty and sex. Lastly, we used emotional pictures, influence varies across sexes.
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