Cognitive efficiency on a match to sample task decreases at the onset of puberty in children

Brain and Cognition 50 (2002) 73–89 www.academicpress.com

Cognitive efficiency on a match to sample task decreases at the onset of puberty in children Robert F. McGivern,* Julie Andersen, Desiree Byrd, Kandis L. Mutter, and Judy Reilly San Diego State University, 6330 Alvarado Ct, 207, San Diego, CA 92120, USA Accepted 19 February 2002

Abstract Electrocortical evidence indicates that a wave of synaptic proliferation occurs in the frontal lobes around the age of puberty onset. To study its potential influence on cognition, we examined 246 children (10–17 years) and 49 young adults (18–22 years) using a match-to-sample type of task to measure reaction times to assess emotionally related information. Based upon the instruction set, subjects made a yes/no decision about the emotion expressed in a face, a word, or a face/word combination presented tachistoscopically for 100 ms. The faces were images of a single individual with a happy, angry, sad or neutral expression. The words were ‘happy,’ ‘angry,’ ‘sad,’ or ‘neutral,’ In the combined stimulus condition, subjects were asked to decide if the face and word matched for the same emotion. Results showed that compared to the previous year, reaction times were significantly slower for making a correct decision at 11 and 12 years of age in girls and boys, the approximate ages of puberty onset. The peripubertal rise in reaction time declined slowly over the following 2–3 years and stabilized by 15 years of age. Analyses of the performance of 15–17 year olds revealed significantly longer reaction times in females to process both faces and words compared to males. However, this sex difference in late puberty appeared to be transient since it was not present in 18–22 year olds. Given the match-to-sample nature of the task employed, the puberty related increases in reaction time may reflect a relative inefficiency in frontal circuitry prior to the pruning of excess synaptic contacts. Ó 2002 Elsevier Science (USA). All rights reserved. Keywords: Puberty; Frontal lobe; Synaptogenesis; Sex difference; Facial expression; Priming; Reaction time; Emotion

1. Introduction The increasing levels of abstract ability that appear at punctuated intervals between infancy and adolescence are assumed to be mediated by structural changes in the brain (Chugani, 1997; Johnson, 1999; Piaget, 1972). Support for this is reflected in the association between frontal lobe development and the ontogeny of abstract abilities in human infants and non-human primates (Diamond, 1991; Rakic, Bourgeois, & Goldman-Rakic, 1994). However, while regions of the frontal, parietal, and *

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temporal cortex, as well as limbic areas, continue to change into late adolescence, little is known in children and adolescents about the specific relationship between these structural changes and cognition (Giedd et al., 1996, Giedd, Castellanos, Rajapakse, Vaituzis, & Rapoport, 1997, 1999; Jernigan, Trauner, Hesselink, & Tallal, 1991; Paus et al., 1999; Sowell, Thompson, Holmes, Jernigan, & Toga, 1999). The non-linear pattern of cognitive development in children correlates well with a cyclical pattern of transient electrocortical coherence among different cortical regions (Fischer et al., 1997; Thatcher, 1992, 1997a). This coherence is believed to stem from the production of new synaptic contacts that have yet to be recruited into functional networks. Major cycles of coherence in overall cortical connection occur at regular intervals with major cycles observed at 1.5–5 years of age, 5–10 years, and 10–16 years, with repetitive subcycles of regional neural connectivity occurring within each major cycle (Thatcher, 1997a). Frontal circuits lag systematically behind posterior regions in their reorganization, raising the possibility that they are recruiting posterior associational areas into a frontal network (Thatcher, 1997b). Although cognitive processing related to specific intellectual skills often depends upon posterior brain regions, it is the prefrontal areas that are critical for the integration of the subprocessing done by distributed local circuits. The binding role of frontal circuitry underlies cognitive capacities related to selective attention, working memory, and planning (Fuster, 1997). The developmental relationship of these capacities to cognitive development is well established, so it is not surprising that the electrocortical pattern of cyclical reorganization of frontal circuitry corresponds well with the appearance of Piaget’s stages of intellectual development (Fischer & Rose, 1997). One of the major cycles of EEG coherence occurs around the general time of puberty onset, which is also a period when sex-related structural changes in gray matter have been observed in cortex (Giedd et al., 1999; Thatcher, 1997a). Throughout the brain, gray matter is comprised of somatodendritic processes that are correlated with synaptic density. Using MRI, Giedd and co-workers (1999) observed a linear increase in gray matter volume in the parietal and frontal regions between 4 years of age and the approximate age of onset for puberty. In girls, the asymptote was at 10.2 years in the parietal cortex and 11.0 years in the frontal cortex. For boys, the asymptotic ages were 11.8 years and 12.1 years for the two respective areas. These age-related sex differences correspond well with the age of the first appearance of secondary sex characteristics (Grumbach & Styne, 1992; Tanner, 1962). During peak periods of synaptic proliferation in a region of cortex, information processing may be less efficient due to an excess number of synaptic contacts that have yet to be pruned (Huttenlocher, 1979; Huttenlocher & Dabholkar, 1997). Therefore, a decline in the functional efficiency of that region might be hypothesized due to a decrease in signal to noise ratio caused by the excess number of synapses. To examine this hypothesis around the time of puberty, we used a match to sample type of task that employs emotionally related stimuli for two classes of items, faces and words. The task places a significant demand on frontal lobe circuitry due to its combined reliance on attention and working memory in order to compare a stimulus with the predefined criteria. However, the nature of the stimuli, as well as the comparison decision, place a relatively low demand on intellectual ability or experience for school age children. The stimuli were faces and words that related to the emotional states of ‘happy,’ ‘angry,’ ‘sad,’ or ‘neutral,’ The two different classes of stimuli were first presented alone. The participants role was to decide if the stimulus presented matched the target emotion previously defined by the instruction set. In a subsequent condition, the participants were presented with a face/word combination, and asked to decide if the two matched. By employing both verbal and non-verbal stimuli pertaining to the same emotional categories, we attempted to access two separate, but overlapping neural pathways processing faces and words (McCarthy, 1999). Due to an excess of

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unincorporated synaptic contacts around the age of puberty onset, we hypothesized that we would observe longer reaction times when the task involved the simultaneous activation of both pathways. Thus, we expected to see significantly longer reaction times at the age of puberty onset in males and females when asked to make a ‘yes’ or ‘no’ decision about whether a face/word combination matched for the same emotion.

2. Methods 2.1. Participants: children The children were drawn from a local private high school and several middle schools. Testing was conducted tested during an 18-month period. The population provided an ethnically diverse group that was devoid of serious learning disabilities and generally homogeneous with regard to middle to upper middle socioeconomic status. Children with identified learning disabilities were screened from the study by the school administration. Each child was asked about medications, handedness, and eyesight. Handedness was assessed by asking the child to demonstrate with which hand they threw a ball, looked though a telescope, and wrote with a pencil. Data were subsequently excluded from analysis for subjects who were not right handed, who were on medication which might interfere with perceptual processing, including antidepressants, and who had any history of learning disabilities or attentional problems. The sample for analysis consisted of 246 children (124 male and 122 female). School policy did not allow direct questions related to puberty or the physiology associated with it. Therefore, we used national estimates of the age of onset from data representing more than 17,000 children in the United States (Grumbach & Styne, 1992; see Herman-Giddens et al., 1997, for discussion of age of onset in different studies and regions). The average age for the onset of puberty in females was 10.6 (
1.8, SD) years compared to 11.2 (
0.7, SD) for boys: the mean age when breast development or male genital enlargement was first evident. The average age of menarche was 12.9 (
1.2, SD) years. 2.2. Participants: young adult Males ðN ¼ 23Þ and females ðN ¼ 26Þ between 18 and 22 years of age attending San Diego State University were individually administered the face and word portions of same test to provide a comparison with late adolescent subjects. Subjects were given course-related research credit for their participation. The inclusion criteria for participation were the same as those used in the sample of children. 2.3. Procedure and apparatus To measure reaction time to process face and word stimuli, we developed a computer based task which presented stimuli tachistoscopically for 125 ms on a 14 in. computer monitor screen. Testing was conducted individually in a separate room. The participants were seated in a chair in front of the screen and viewed the stimuli through a 12 in:  12 in:  15 in: black box placed 15 in. from the screen. The box was designed to reduce environmental distraction and to help focus attention on the task. Subjects were presented three types of black and white stimuli; (1) photographic images of a face with a happy, angry, neutral or sad expression, (2) the words ‘Happy,’ ‘Angry,’ ‘Neutral,’ or ‘Sad,’ or (3) images which combined one of the fours faces with one of the four words. The four face images were obtained using a scanner from the published work of Suberi and McKeever (1977). They were of a single individual wearing a hood to minimize sex-related characteristics.

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The stimuli were 2:5 in:  2:5 in: in size and appeared in the center of the screen. A plus sign appeared in the center of the screen for 500 ms immediately preceding the stimulus onset to alert the subject on each trial. The stimuli were presented in blocks of 16 trials, with a brief rest between blocks. At the beginning of each block for faces and words, the subject was given a different emotion upon which to base their decision. For the Face/Word condition, subjects were asked to make a decision whether the two stimuli matched for the same emotion. Faces were presented for blocks 1–4, words for blocks 5–8, and face/word combinations for blocks 9–12. In all, the test consisted of 192 trials. Within each block, the intertrial interval averaged 2500 ms, with a range of 2000–3000 ms. The reaction time was measured by the computer, which calculated the time from stimulus onset to the activation of a voice key. Responses longer than 2000 ms were not used for analysis. For the first block, subjects were given the following instructions, ‘If the face is angry, please answer yes, to any other expression, say no. Please answer as quickly as you can.’ For the second block, the subject was instructed to look for the happy face, for the third, the neutral face, and for the fourth, the sad face. For blocks 5–8, the subjects were instructed to look for the words ‘Angry,’ ‘Happy,’ ‘Neutral,’ or ‘Sad’ in that order across the 4 blocks. For blocks 9–12, subjects were simply instructed to say ‘yes’ if the stimuli matched and ‘no’ if they did not. Within each of the 4 block segments for the face and word presentations, and face/ word combinations, there were 16 conditions that reflected all possible combinations of what the subject was seeking and what was actually presented. These are shown below in Table 1. 2.4. Data analysis For each condition, the reaction times for each subject were averaged for correct answers (yes or no) for each of the 16 combinations shown in Table 1. Data for a given trial were not used in subsequent analyses if the mean reaction time was two standard deviations from the group mean of the subject’s age and sex. Subjects were grouped by age in the analyses using 7 yearly increments (10, 11, 12, 13, 14, 15, and 16). Due to large differences in the reaction times among the 3 classes of stimuli (Face, Word, and Face/Word combination), each class of stimuli was analyzed separately. Data from the face alone and word alone conditions were analyzed in separate 2 ðSexÞ  6 ðAgeÞ  4 ðTarget emotionsÞ  4 ðEmotion shownÞ ANOVAs with repeated measures over the last two factors. Data from the Face/Word combination were analyzed using a 2 ðSexÞ  6 ðAgeÞ  16 ðface=word combinationÞ ANOVA. Post hoc analyses were conducted using Newman–Keuls multiple range tests. For the within-subject analysis, all subjects did not have data from all 48 conditions due either to (1) errors, or (2) elimination of data in a specific condition that was greater than two standard deviations from the mean of their sex and age group for that condition. This reduced the number of subjects making correct decisions in all 48 conditions to the following: Face alone, 192; Word alone, 230; Face/Word Table 1 Instructional conditions for each of the four blocks of stimuli used for faces and words Seek Angry ¼ Trials 1–16; 65–80 Seek Happy ¼ Trials 17–32; 81–96 Seek Neutral ¼ Trials 33–48; 97–112 Seek Sad ¼ Trials 49–64; 113–128 The following were the 16 possible ‘seek/see’ combinations for the face and word conditions. AA Angry/Angry HA Happy/Angry NA Neutral/Angry SA Sad/Angry AH Angry/Happy HH Happy/Happy NH Neutral/Happy SH Sad/Happy AN Angry/Neutral HS Happy/Sad NN Neutral/Neutral SN Sad/Neutral AS Angry/Sad HN Happy/Neutral NS Neutral/Sad SS Sad/Sad For the face/word condition, each of the 16 face and word combinations appeared four times over the 64 trials in the 4 blocks. Total trials ¼ 192 (Face alone, n ¼ 64; Word alone, n ¼ 64; Face/Word, n ¼ 64).

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Combo, 211. The participants in the 10–11 and 11–12 year old groups provided the majority of cases with missing data. While overall error rates within the 3 stimulus conditions were greatest in the face alone condition, the average in all three conditions at each age for correct answers was greater than 85%.

3. Results 3.1. Children An overall ANOVA was performed on the collapsed reaction times in each stimulus condition in a 2 ðSexÞ  3 ðconditionÞ with repeated measures over the last factor. The analysis conditions revealed a large difference in reaction time between the conditions (F ½2; 494 ¼ 1474; p < :0001). The average reaction time for correctly identifying words was significantly shorter than for faces or face/word combinations ðp < :0001Þ. The reaction time for the face condition was significantly shorter than the face/word match condition ðp < :0001Þ. The analysis also revealed a significant main effect for sex (F ½1; 247 ¼ 4:29; p < :05). The collapsed means for each stimulus condition are show below in Table 2. Each stimulus condition was subsequently analyzed separately using age and sex as factors. The results revealed a significant increase in reaction time for both the face and word conditions at the onset of puberty. For girls, this increase was evident in the 10–11 year old group. For boys, the increase was evident in the 11–12 year old group. A similar trend was observed in the combined Face/Word condition, but no significant main effect of Sex or interactions with Sex were observed. Results for the Face and Word conditions are shown in Fig. 1. Examples of the puberty-related increase in reaction time are shown in Fig. 2. Fig. 3 depicts the comparison of reaction time for the year preceding the age of puberty onset. Statistical details are described below. The analysis reaction times when faces were presented alone revealed significant main effect of Sex (F ½l; 180 ¼ 5:74; p < :05); Age (F ½5; 180 ¼ 13:37; p < :0001); Target Emotion (F ½3; 540 ¼ 55:85; p < :0001); and Emotion Shown (F ½3; 540 ¼ 172:38; p < :0001). Significant interactions included the following: Sex  Age (F ½5; 180 ¼ 2:49; p < :05); Target Emotion  Age (F ½15; 540 ¼ 4:72; p < :0001); Target Emotion  Age  Sex (F ½15; 154 ¼ 1:79; p < :05); Emotion Seen  Age (F ½1; 180 ¼ 5:74; p < :05); Emotion Shown  Target Emotion (F ½9; 1620 ¼ 14:81; p < :0001); and Emotion Shown  Target Emotion  Age  Sex (F ½45; 1620 ¼ 1:60; p < :01). The analysis of the Word alone condition revealed significant main effects of Sex (F ½1; 218 ¼ 9:15; p < :001); Age (F ½5; 218 ¼ 11:74; p < :0001); Target Emotion (F ½3; 65424:25; p < :0001), and Emotion Shown (F ½3; 654 ¼ 32:92; p < :0001). Significant interactions included Target Emotion  Age (F ½15; 5654 ¼ 1:86; p < :05); Emotion Shown  Sex (F ½3; 654 ¼ 3:23; p < :05); Emotion Shown  Target Emotion (F ½9; 1962 ¼ 20:91; p < :0001); and Emotion Seen  Target Emotion  Age (F ½45; 1962 ¼ 1:60; p < :01); and Emotion Seen  Target Emotion  Age  Sex (F ½45; 1962 ¼ 1:39; p < :05).

Table 2 Reaction time in milliseconds (mean and SEM) collapsed across age and trials within each stimulus condition Stimulus

Males

Female

Face Word Face/Word

849 (15.3) 588 (11.5) 971 (17.2)

881 (14.4) 640 (12.7) 1006 (17.0)

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Fig. 1. Reaction time (mean and SEM) for correct responses in males and females at 10–17 years of age. Data shown are collapsed across each stimulus type.

The Face/Word combination analysis revealed significant main effect of Age (F ½5; 199 ¼ 7:35; p < :0001) and Trial (F ½15; 2985 ¼ 55:74; p < :0001), as well as a significant interaction between Trial  Age (F ½75; 2985 ¼ 1:32; p < :05).

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Fig. 2. Reaction times (mean and SEM) for correct responses in three representative stimulus conditions. In each ‘seek/shown’ condition, there was a target emotion to identify and the actual emotion associated with the stimulus. In the ‘‘Happy/Angry’’ condition, the target was ‘happy’ and the face or word shown was ‘angry.’ Three to five presentations were shown for each ‘seek/shown’ condition.

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Fig. 3. Comparison of reaction times (mean and SEM) for the year preceding to the average age of puberty onset. Upper panel compares the data collapsed across the 16 conditions for each stimulus. Lower panel compares data for representative conditions shown in Fig. 2. The ‘*’ indicates a significant difference between the prepuberty reaction time compared to the reaction time at the average age of puberty onset.

Post hoc analyses revealed that age-related changes were absent in all of the three stimulus conditions in the 15–17 year olds subjects. Therefore, further analyses were conducted in these subjects to examine sex differences in making a decision about specific emotional categories. The responses for decisions under ‘primed’ conditions (i.e., reaction time for identifying the target emotion) were analyzed separately from responses to the same stimulus under ‘non-primed’ conditions. The average reaction

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Fig. 4. Reaction times (mean and SEM) for correct responses in both 15–17 and 18–22 year old males and females. Panels A and B show reaction time for each ‘seek/shown’ condition for face stimuli. Panels C and D show reaction times for the word stimuli. A ‘+’ indicates a significant sex differerence within a specific stimulus condition ðp < :05Þ. An ‘*’ indicates a significant priming effect ðp < :05Þ, as defined when the non-target stimulus (i.e., ‘Happy/Angry’) was compared to the target expected stimulus condition (i.e., Happy/Happy).

time for each ‘non-primed’ stimulus was compared with its ‘primed’ counterpart in a 2 ðSexÞ  2 ðprimed vs non-primedÞ ANOVA with repeated measures over the second factor. As shown in Fig. 4A, reaction times in the Face alone condition were longer for females than males to correctly identify happy (F ½1; 64 ¼ 5:87; p < :02) and sad (F ½1; 64 ¼ 6:08; p < :02) expressions. A main effect for priming was observed only in the happy condition (F ½1; 64 ¼ 12:80; p < :001). Post hoc analyses revealed a significant sex effect for the sad expression for both primed and non-primed conditions ðp < :05Þ. For the happy expression, a significant sex effect was observed only in the non-primed condition. For priming in the happy face condition, a significant effect was found only in females ðp < :05Þ.

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Fig. 4. (continued)

In the Word condition, females exhibited significantly longer reaction times than males for all four emotions: Happy (F ½1; 64 ¼ 8:22; p < :01); Angry (F ½1; 64 ¼ 4:27; p < :05); Sad (F ½1; 64 ¼ 8:82; p < :01); Neutral (F ½1; 64 ¼ 16:09; p < :005). Post hoc analyses revealed significant sex effects under both primed and non-primed conditions for all four words ðp < :05Þ. However, no significant effects of priming were detected for any of the word stimuli. Results are shown in Fig. 4B. When subjects were presented with the combined Face/Word stimuli, significant sex effects were observed only when the face was sad, irrespective of the face for which they were looking for (F ½1; 64 ¼ 4:56; p < :05). Post hoc tests revealed that females were significantly slower than males under both match and non-match conditions ðp < :05Þ. Significant positive priming was observed for both sexes when the Face/Word combination matched for happy (F ½1; 64 ¼ 148:02; p < :0001). When the Face/word combination was angry, there was a significant main effect for priming (F ½1; 64 ¼ 5:20; p < :02) as well as a significant interaction between sex and priming (F ½1; 64 ¼ 6:09; p < :02). Negative priming was found in males ðp < :05Þ when the face was angry, but the word was not. Results are shown in Fig. 4C.

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Fig. 4. (continued)

3.2. Young adults In the 18–22 year oldgroup, there was no significant effect of gender for either face or word stimuli when the data were analyzed by ANOVA with repeated measures over the face/word condition, emotion shown, and target emotion. The face and word stimuli in this group were subsequently compared with responses from 15–17 year olds in a 2 ðAgeÞ  2 ðSexÞ  2 ðcondition; face= wordÞ  4 ðemotion shownÞ  4 ðtarget emotionÞ ANOVA with repeated measures over the last 3 factors. Results revealed significant main effects of face/word condition (F ½1; 103 ¼ 755:45; p < :0001), emotion shown (F ½3; 309 ¼ 173:83; p < :0001), and target emotion (F ½3; 309 ¼ 7:83; p < :0001). Significant interaction were observed between Age  Sex (F ½1; 103 ¼ 5:28; p < :03), Age  Sex  Target Emotion (F ½3; 309 ¼ 3:05; p < :03), Condition  Target Emotion (F ½3; 309 ¼ 20:39; p < :0001), Emotion Shown  Target Emotion (F ½3; 309 ¼ 121:82; p < :0001), Age  Face=WordCondition  Emotion (F ½3; 309 ¼ 3:33; p < :02), Age  Emotion Shown  Target Emotion (F ½3; 309 ¼ 2:04; p < :04), and Face=Word Condition 

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Fig. 4. (continued)

Emotion Shown  Target Emotion (F ½9; 927 ¼ 12:78; p < :0001). Data are shown in Fig. 4.

4. Discussion Our results reveal a significant rise in reaction time to process emotionally related stimuli around the average age of puberty onset. Although male and female reaction times were similar at 10 years of age, there was a 10–20% rise in reaction time to make a correct decision by the average age of puberty onset when compared to the preceding age group within each sex. Reaction time decreased in boys between 10 and 11 years of age, followed by an increase between 12 and 13 years of age. After this point, the linear downward trend continued but was reset from the new level established at puberty onset. In females, reaction time increased between 11 and 12 years of age, followed by a gradual decrease over the next few years. Because of the

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limited data from girls before the average age of puberty onset, it is not clear whether the similar rise in females also reflects a reset in this age-related trend. Although reaction time slowed at puberty onset, error rates did not increase, suggesting that neural inefficiency rather than cognitive impairment may underlie the increase in reaction time. The increase was also not associated with increased task complexity. We anticipated observing a puberty-related effect only in the Face/Word condition, the condition where competing neural circuits were involved in the match/ no-match decision. However, significant effects were observed only in the two simpler conditions that involved the face or word presented alone. These stimuli were neither intellectually challenging, nor difficult to discern. Therefore, observing the hypothesized effect under these conditions suggests that puberty-related processes impair efficiency rather than cognition on this type of task. Effect size may help to explain the lack of a significant effect in the more complex word/face match condition. The overall size effect is relatively small, and therefore the increased variance associated with the Face/Word complexity may have masked the effect compared to the other two simpler conditions. Given that the rise in reaction time involved both linguistic and non-linguistic stimuli, we can assume that that puberty-related change involves cognitive systems that bind information from local processing related to linguistic and facial processing. However, since both classes of stimuli employed in this study relate directly or indirectly to emotional state, we do not know whether the pubertal rise in reaction time will generalize to more abstract cognitive processing, or to stimuli that have little emotional content. To further address this, it will be helpful to test conditions where children are asked to make a decision about simple, non-emotional stimuli such as the word ‘table’ or to decide whether an image matches a neutral stimulus such as a table. Determining whether the rise in reaction time extends to non-emotional stimuli may also shed some light on the possible differential development of the prefrontal cortex during puberty. The prefrontal cortex has two subdivisions that differentiate with a bias toward social/emotional assessment vs abstract/logical reasoning (Fuster, 1997). The orbitofrontal region, which has strong reciprocal connections with the cingulate, amygdala, and other limbic structures, plays an important role in the assessment of social relationships, as well as planning and control of our social behavior (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999; Eslinger, 1998). In contrast, the dorsolateral region of the prefrontal area is more involved in abstract reasoning (Rakic et al., 1994). Current studies have not addressed whether the structural changes in frontal lobes during puberty are relatively specific to either of these subdivisions in the prefrontal area. Proliferative and pruning mechanisms acting on frontal circuitry may account for the rise in reaction observed in the present study. Synaptic proliferation, followed by pruning, is assumed to be a coupled mechanism in the developing brain whereby genetic programming and environmental influences interact to shape cognitive development (Greenough, Black, & Wallace, 1987; Huttenlocher, 1979). In infants, there is good evidence to support this mutual relationship (Diamond, 1991; Johnson, 1999; Mrzljak et al., 1990), but neurobehavioral studies in frontal cortex at later developmental periods are few. However, supporting evidence comes from electrophysiological studies of children (Thatcher, 1992, 1997b). These data indicate that there are several waves of cortical proliferation occurring between infancy and early adulthood, with a prominent wave occurring around the time of puberty. This is consistent with evidence showing that gray matter volume reaches asymptote in the frontal cortex at the approximate ages at which we observed the increase in reaction time (Giedd et al., 1999). Following asymptote, there was a decline in gray matter volume over the next few years, leading to the suggestion that pruning during this period may be related to actions of sex steroid hormones.

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This proposal is supported by studies in non-human primates indicating that steroid hormones at puberty induce reorganization of both intrinsic and associational neural circuits in the prefrontal cortex (Woo, Pucak, Kye, Mattis, & Lewis, 1997). Other animal work has also found an influence of sex steroids on cortical and limbic development during the pubertal period (Matsumoto, 1991; Morse, Scheff, & DeKosky, 1986; Roselli & Klosterman, 1998). However, although sex steroid receptors are broadly distributed in the neocortex (Sar, Lubahn, French, & Wilson, 1990; € sterland & Hurd, 2001) the evidence in humans for sex steroids actions during puO berty on brain and behavior remains inferential. In a broad review of the role of hormones on adolescent behavior, Buchanan, Eccles, and Becker (1992) found only indirect support for the influence of hormonal factors on social behaviors and emotional lability. And non-hormonal factors appeared to be more important in areas such as self-esteem and perceived confidence. The issue remains clouded due to the lack of human studies that have directly assessed the association between changing hormone levels and cognition during puberty. The proposition that hormonal actions on brain structures may underlie cognitive changes in adolescents is not recent (Epstein, 1978; McCall, Meyers, Hartman, & Roche, 1983). Epstein (1978) conducted the first large-scale study that suggested a role for hormones in influencing cognitive processes in adolescents. He found an association between head circumference and general cognitive skills across the adolescent period. Periods of cranial growth during adolescence, reflecting the trophic influence of sex steroids on bone growth, were significantly correlated with declines in cognitive performance. It was assumed that steroid influences on bone growth were paralleled by increased synaptic density in brain. Although the relationship of brain development to cranial growth at puberty has been questioned (McCall et al., 1983), the recent findings of Giedd et al. (1999) showing sex differences in frontal and parietal gray matter at the onset of puberty support the basic premise that hormonal changes at puberty can induce structural changes in brain. In contrast to Epstein’s findings, a study of 253 male and female adolescents in grades 6–8 found no evidence for a puberty-related dip in performance on sexually dimorphic tasks (Crockett & Petersen, 1987; Petersen, 1988). The authors used tasks involving formal reasoning, spatial ability, and verbal fluency that generally exhibit a male or female bias in performance. As expected, their results showed significant overall sex effects on spatial and verbal abilities, favoring males and females, respectively. Performance on both tasks exhibited a linear improvement with age, with similar improvements for both sexes. Reasoning ability also exhibited a similar linear improvement across age in both sexes. However, no age-related drop in performance emerged around puberty onset in any of the tasks, contrary to what would be predicted from Epstein’s hypothesis. The type of task employed may be important to detect changes in cognitive processing related to puberty. Several studies have found a disruption in the recognition of unfamiliar faces at the onset of puberty (Carey, Diamond, & Woods, 1980; Diamond, Carey, & Back, 1983; Ellis, 1990). Carey et al. (1980) tested groups of children for recognition of unfamiliar faces at 7, 9, 10, 11, 12, 14, and 16 years of age. Their results revealed linear improvement in children’s ability to encode faces until 11 years of age. At this point, performance dropped significantly, with no further improvement observed until 14–16 years of age. A second finding from the present study is a sex difference in the reaction time of 15–17 year olds. Females took significantly longer than males to assess both facial and linguistic stimuli related to emotion. The effect was present for happy and sad facial stimuli, as well as for all four linguistic stimuli. Since these sex differences were no longer present in 18–22 year olds, they appear to reflect a transient difference in functional brain organization during late adolescence. The functional significance of

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this transient sex difference is unclear, particularly because it does not involve accuracy in making a correct decision. Observing a sex difference in such a simple task raises the possibility of a transient refining organizational influence of steroids on the perceptual systems mediating cognitive sex differences observed in more complex tasks. Steroid actions in early development organize neural circuits underlying cognitive sex differences in humans (Reinisch & Sanders, 1992). But their amplification or further refinement by hormones during puberty is an intriguing possibility suggested by the sex difference in processing speed of late adolescents. Results from a number of studies indicate that information processing of some types of stimuli involves differential activation of neural circuits in men and women. For instance, studies in adults indicate that emotional and verbal encoding in women is more broadly distributed across limbic and cortical networks compared with men. Females performing a language task, or processing linguistic stimuli, exhibit broader neural activation of the neocortex than males (Gur, Gur, Obrist, & Hungerbuhler, 1982, 2000; Shaywitz et al., 1995). Females also report more emotionally laden detailed information in autobiographical narratives than males, and unconscious associations to visual stimuli are more accessible to conscious recall (Cowan & Davidson, 1984; Friedman & Pines, 1991; McGivern et al., 1997, 1998 Silverman & Eals, 1992). Anatomically, sex differences have been observed in cortical gray matter volume, as well as in the development of lateralization in the size of the hippocampus and amygdala of late adolescents and adults (Giedd et al., 1996; Gur et al., 1999). To what degree hormonal actions during adolescence contribute to these organizational effects is an essential question for understanding the neuropsychology of cognitive sex differences. In summary, our results show a decrement in cognitive efficiency at the onset of puberty. This age-related dip may represent a functional marker of the phase shift between proliferation and the onset of pruning. Defining the parameters of cognitive and emotional processing that exhibit this dip in neural efficiency may help to optimize the role of experience in the pruning process and its attendant impact on intellectual and emotional growth during adolescence. Finally, if neurocognitive development is a process of cyclical elaboration of processing complexity, drops in cognitive efficiency related to executive function in the frontal lobe may mark the onset or peak of cycles that occur at younger ages as well.

Acknowledgments Funding was provided by the San Diego State University Foundation. The authors would like to thank Tina King, Patrick Huston, Amy Saba, Paula Vickery, and Diane Willis for help with the collection of the data. We would also like to express our gratitude to Graham Wideman for developing the programming, and to Jerrold Miles, the Headmaster of Francis Parker School, whose generous assistance and encouragement made the study possible.

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