ELSEVIER Neuropsychologia 44 (2006) 2037-2078 IWUROPSYCHOLOGIA

ELSEVIER Neuropsychologia 44 (2006) 2037-2078 IWUROPSYCHOLOGIA www elsevier comilocateineumpsychologia Development of cognitive control and executive functions from 4 to 13 years: Evidence from manipulations of memory, inhibition, and task switching Matthew C. Davidson a'b, Dima Amso a, Loren Cruess Anderson c, Adele Diamond d,* Sackler Institute for Developmental Psychobiologx frill Medical College of Cornell University; New York. NY. USA b Department of Psychologx University of Massachusetts. Amherst. MA. USA Shrive, Center. University of Massachusetts Medical School, Waltham. MA. USA d Department of Psychiatrx University of British Columbia & Division of Child & Adolescent Psychiatty, BC Children's Hospital. Vancouver. Canada Received 20 November 2005: received in revised form 7 February 2006: accepted 10 February 2006 Available online 31 March 2006 Abstract Predictions concerning development, interrelations, and possible independence of working memory, inhibition, and cognitive flexibility were tested in 325 panicipants (roughly 30 per age from 4 to 13 years and young adults.. 50% female). All were tested on the same computerized battery. designed to manipulate memory and inhibition independently and together. in steady state (single-task blocks) and during task-switching. and to be appropriate over the lifespan and for neuroimaging (MARI). This is one of the first studies, in children or adults, to explore: (a) how memory requirements interact with spatial compatibility and (b) spatial incompatibility effects both with stimulus-specific rules (Simon task) and with higher-level, conceptual rules. Even the youngest children could hold information in mind, inhibit a dominant response. and combine those as long as the inhibition required was steady-state and the rules remained constant. Cognitive flexibility (switching between rules), even with memory demands minimized, showed a longer developmental progression. with 13-year-olds still not at adult levels. Effects elicited only in Mixed blocks with adults were found in young children even in single-task blocks: while young children could exercise inhibition in steady state it exacted a cost not seen in adults, who (unlike young children) seemed to re-set their default response when inhibition of the same tendency was required throughout a block. The costs associated with manipulations of inhibition were greater in young children while the costs associated with increasing memory demands were greater in adults. Effects seen only in RT in adults were seen primarily in accuracy in young children. Adults slowed down on difficult trials to preserve accuracy: but the youngest children were impulsive; their RT remained more constant but at an accuracy cost on difficult trials. Contrary to our predictions of independence between memory and inhibition, when matched for difficulty RT correlations between these were as high as 0.8. although accuracy correlations were less than half that. Spatial incompatibility effects and global and local switch costs were evident in children and adults, differing only in size. Other effects (e.g.. asymmetric switch costs and the interaction of switching rules and switching response-sites) differed fundamentally over age. O 2006 Elsevier Ltd. All rights reserved. Keywords: Task switching: Inhibition: Working memory: Simon effect: Asymmetric switch costs: Global and local switch costs: Stimulus—response compatibility: Development: Children: Frontal lobe Mature cognition is characterized by abilities that include being able: (a) to hold information in mind, including compli- cated representational structures, to mentally manipulate that information, and to act on the basis of it, (b) to act on the basis of choice rather than impulse, exercising self-control (or self- regulation) by resisting inappropriate behaviors and responding • Corresponding author at: Department of Psychiatry. University of British Columbia. 2255 Wesbrook Mall. Vancouver. BC. Canada V6T 2AL Tel.: +1 604 822 7220: fax: +1 604 822 7232. E-mail address: adele.diamondaubc.ca (A. Diamond). 0028-3932(8 — see front matter O 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2006.02.006 appropriately, and (c) to quickly and flexibly adapt behavior to changing situations. These abilities are referred to respec- tively as working memory, inhibition, and cognitive flexibility. Together they are key components of both "cognitive control" and "executive functions" and have been studied in a wide vari- ety of experimental paradigms with diverse subject groups. Our battery of interrelated tasks enabled us to indepen- dently and systematically vary demands on these abilities and to track their development across a wider age range than hereto- fore investigated using the same measures at all ages. Hav- ing measures that span a wide age range is important given the protracted developmental progressions of many executive EFTA01098878 2038 MC. Davidson e at /Neumps)rhologia 44 (2006)2037-2078 function and cognitive control skills. While some cognitive abilities develop early, executive functions do not reach their peak until early adulthood (DeLuca et al., 2003; Diamond, 2002; Fischer, Biscaldi, & Gezeck, 1997; Harnishfeger & Pope, 1996; Kail, 1991abc; Kail & Salthouse, 1994; Luciana & Nelson, 2002; Luciana, Conklin, Hooper, & Yarger, 2005; Luna, Garver, Urban, Lazar, & Sweeney, 2004; Lyons-Warren, Lillie, & Hershey, 2004; Munoz, Broughton, Goldring, & Armstrong, 1998; Zelazo, Craik, & Booth, 2004). Each test in our battery can be performed by children as young as 4 years; yet adults still find many of them challenging. The entire battery takes less than 30 min to complete. These tests are also designed to be appropriate for testing nonhuman primates and for neu- roimaging research using functional magnetic resonance imag- ing (fMRI) (Diamond, O'Craven, & Savoy, 1998; O'Craven, Savoy, & Diamond, 1998). Across this wide age span, our battery provides within- subject measures of two classic paradigms in cognitive psy- chology, the Simon task and task switching. In the Simon task paradigm, a non-spatial aspect of the stimulus (such as its color or identity) is relevant and its spatial location is irrele- vant. Nevertheless, the well-replicated finding in adults is that responses are faster and more often correct when the stimu- lus and response are on the same side than when they are on opposite sides (the Simon effect, also called spatial incompati- bility or stimulus—response compatibility; e.g., Craft & Simon, 1970; Fitts and Seger, 1953; Hommel, 1995; Hommel, Proctor, & Vu, 2004; Lu & Proctor, 1995; Simon & Small, 1969; Simon, 1990; Simon & Berbaum, 1990). This effect indicates: (a) the influence of an irrelevant stimulus attribute on performance and (b) a prepotent tendency to respond on the same side as the stimulus (confirmed at the neuronal level [see Georgopoulos, 1994; Georgopoulos, Lurito, Petrides, Schwartz, & Massey, 19891 and with lateralized readiness potentials [Valle-Inclan, 19961) which must be inhibited when the locations of stimu- lus and response are incompatible. It thus provides insight into an aspect of inhibitory control. A finding that the Simon effect decreases over a certain age range provides evidence for when developmental improvement in that aspect of inhibition occurs and insight into when maturational changes in the neural sys- tem underlying that might be occurring. That neural system overlaps substantially with the neural system activated during Stroop interference and other cognitive control paradigms. It includes the anterior cingulate, lateral prefrontal cortex (dorso- lateral and ventrolateral), pre-SMA, premotor cortex, posterior and superior parietal cortex, inferior temporal cortex, the insula, and precuneus (Bush, Shin, Holmes. Rosen, & Vogt, 2003; Dassonville et al., 2001; Fan, Flombaum, McCandliss, Thomas, & Posner, 2003; lacoboni, Woods, & Mazziotta, 1998; Liu, Banich, Jacobson, & Tanabe, 2004; Maclin Gratton, & Fabiani, 2001; Peterson et al., 2002; Thomas et al., 1999; Wager & Smith, 2003). We investigated spatial incompatibility effects both decreas- ing and increasing the working memory requirements tradition- ally required for Simon tasks. We decreased it in one case by providing icons depicting stimuli A and B over their respective response-sites so that which response goes with which stimulus did not have to be held in mind and in another case by using stimuli (Arrows) that pointed to where to respond. We increased the working memory requirements by introducing conceptual rules, where the correct response required mental manipulation. Instead of a rule being "for A press left:' a rule was "for A press on the side opposite A:' Thus, in addition to activating the rules associated with the two stimuli (the memory require- ment in standard Simon tasks), participants had to instantiate the appropriate rule for the particular spatial location of the stimulus on each trial. Task-switching paradigms target the ability to flexibly shift from one mindset to another, often times acting according to rules that would be incompatible with the other mindset. This has been studied extensively in adults (e.g., Allport, Styles, & Hsieh. 1994; Jersild, 1927; Meiran, Gotler, & Perlman, 1996; Monsell & Driver, 2000; Rogers & Monsell, 1995; Meiran et al., 2000a,b; Meiran, 2005; Spector & Biederman, 1976; Sudevan & Taylor, 1987), including the elderly (e.g., Kramer, Hahn, & Gopher, 1999; Mayr, 1996; Meimn, Gotler, & Perlman, 2001), and in various clinical groups (e.g., Aron, Sahakian, & Robbins, 2003; Brown & Marsden, 1988; Downes et al., 1989; Flowers & Robertson, 1985; Hayes, Davidson, Rafal & Keele, 1998; Mecklinger, von Cramon, Springer, & Mantles- von Cramon, 1999; Rogers et al., 1998). However, to date, only a handful of studies have looked at task switching in chil- dren (Cepeda, Kramer, & Gonzalez de Sather, 2001; Cohen, Bixenman, Meiran, & Diamond, 2001; Crone, Bunge, Van der Molen, & Ridderinkhof, in press; Crone, Ridderinkhof, Worm, Somsen, & van der Molen, 2004; Reimers & Maylor, 2005; Zelazo, Craik, & Booth, 2004). Switching is fundamentally difficult and a paradigmatic instance of when top-down executive control is required because generally it cannot be done "on automatic:' It taxes both working memory and inhibition (the newly-relevant rules and stimulus-response relations must be activated and the previously -relevant ones suppressed). One cannot get in the "groove" of repeatedly doing the same thing or staying in the same mindset because periodically one will have to change that. A groove is a good analogy because it takes effort to climb over the banks of the groove (the mindset) one is in and settle, however temporarily, into another grove. Neuroimaging studies confirm that task-switching (as opposed to continuing to do the same task) activates the neural system associated with executive func- tion and top-down cognitive control, that is lateral prefrontal cortex (dorsolateral and ventrolateral), inferior frontal junction (IFJ) and premotor cortex, pre-SMA and the anterior cingu- late, and the insula and cerebellum (Brass et al., 2003; Brass, Derrfuss, Forstmann, & von Cramon, 2005; Braver, Reynolds, & Donaldson, 2003; Crone, Wendelken, Donohue, & Bunge, 2005; DiGirolamo et al., 2001; Dove, Pollmann, Schubert, Wiggins, & von Cramon, 2000; Dreher & Berman, 2002; Dreher & Grafman, 2003; Kimberg, Aguirre, & D'Esposito, 2000; Meyer et al., 1998; Omori et al., 1999; Pollmann, 2001; Sohn, Ursu, Anderson, Stenger, & Carter, 2000; Sylvester et al., 2003; Wager, Reading, & Jonides, 2004). Consistent with this, patients with frontal cortex damage are impaired at switching between tasks (Mon, Monsell, Sahakian, & Robbins, 2004; Diedrichsen, Mayr, EFTA01098879 M.C. Davidson es nl. /Neuropsychologia 44 (2006)2037-2078 2039 Dhaliwal, Keele. & Ivry, 2000; Keele & Rafal, 2000; Owen et al., 1993; Rogers et al., 1998; Shallice & Burgess, 1991). We report here on the developmental progression in almost 300 children from 4 to 13 years of age and the performance of young adults for comparison, all tested on the same test battery. Various manipulations exploited task switching and spa- tial incompatibility effects, with and without an added memory component, or taxed memory without taxing inhibition or task switching, enabling us to test predictions concerning interre- lations, independence, and the developmental progressions of working memory (how much information you must hold in mind and how many steps must be mentally executed using that information), inhibition (resisting an incorrect response you are inclined to make in order to make the correct response), and cognitive flexibility (switching between tasks or rules). The pre- dictions we tested were generated from hypotheses concerning inhibition and working memory and hypotheses concerning cog- nitive flexibility and task switching. 1. Hypotheses relevant to inhibition and working memory We hypothesized that inhibition would exact a greater relative cost for young children than for older children or young adults, and thus predicted that inhibitory demands would account for a greater proportion of the variance in children's performance than in adults, and the more so the younger the child. In young adults, in whom inhibitory control is more mature, we hypothesized that memory demands would exact a greater cost than inhibitory demands. Because we hypothesized that inhibitory control is extremely problematic for very young children, we predicted they would perform poorly on all trials requiring inhibition (Incongruent trials and switch trials) and that those effects would be addi- tive. We predicted that older children and adults would show the same "asymmetric switch costs" (a greater relative switch cost for switching to the easier [Congruent] condition) previ- ously reported in adults (Allport & Wylie, 2000; Allport et al., 1994; De long, 1995; Kleinsorge & Heuer, 1999; Los, 19%; Stoffels, 1996; Wylie & Allport, 2000). Further, for slightly older children, who are beginning to exercise better inhibitory control, doing so should require greater effort than in older participants. Hence, we predicted that undoing that inhibition (switching back to making a dominant response) should exact a greater cost in those children than in adults. Thus, we pre- dicted that beginning after 6 or 7 years, asymmetric switch costs would be larger in younger than older participants, but that the youngest children would show an opposite pattern of asymmetry. The ability to simply hold items in mind (without any added requirement to manipulate that information or exercise inhibi- tion) develops early, is robust even in preschoolers, and shows little improvement with age (Brown, 1975; Dempster, 1985; Diamond, 1995). Given the early maturation of the ability to hold items in mind, we predicted that although it would be harder for everyone to hold more items in mind than fewer, the relative difficulty of that would not change over age. Finally, Diamond (1991, 2002) and others (Anderson & Spellman, 1995; Gemsbacher & Faust, 1991; Hasher, Stoltzfus, Zacks, & Rypma, 1991) have hypothesized that working mem- ory and inhibition are separable functions. This is consistent with the results of the factor analyses of Miyake et al. (2000) that found working memory and inhibition to be moderately corre- lated but clearly separable. Many scholars, however, have argued that there is no need to postulate an inhibitory function separate from working memory and have produced neural network mod- els consistent with that (Cohen, Dunbar, & McClelland, 1990; Kimberg & Farah, 1993; Miller & Cohen, 2001; Morton & Munakata, 2002; Munakata, 2000). Given that we hypothesized that working memory and inhibition are independent, we pre- dicted that performance on tasks that tax primarily memory or primarily inhibition would not be highly correlated, and tested this for relatively easy tasks and for relatively difficult tasks requiring primarily memory or primarily inhibition, matched on difficulty. 2. Hypotheses relevant to cognitive flexibility and task switching Diamond (1990, 1991, 2002) has long maintained that it is the conjunction of simultaneous demands on holding informa- tion in mind and inhibition that is truly difficult, especially if one's mental settings have to be continually re-set because the task changes. We thus predicted that the most difficult condition at all ages would be the one that taxes inhibition and memory in a switching context, where top-down executive control is con- tinually required, and that that would be even more difficult than having to hold three times as much information in mind but with no inhibition or switching component. Further, since we hypoth- esized that switching is so difficult, we predicted that having to switch between task sets would show a long developmental pro- gression even when memory demands are minimized. Diamond has recently theorized that several seemingly inde- pendent findings in cognitive psychology can be integrated under the hypothesis that the brain and mind tend to work at a grosser level, and only with effort, or more optimal functioning, work in a more selective manner (a theory Diamond has called "all or none" (Diamond, 2005, in preparation)). For example, it is easier to take into account all salient aspects of a stimulus than only some of its properties. Indeed, it is difficult to ignore irrele- vant properties of an attended stimulus, as the Simon effect and children's difficulties on card sorting tasks so amply demon- strate (Diamond, Carlson, & Beck, 2005; Kirkham, Cruess, & Diamond, 2003). Another finding that fits under the all or none rubric is that it is easier to inhibit a dominant response all the time than only some of the time. One of the most demanding cognitive require- ments is to switch back and forth, to overcome inertial tendencies favoring staying in the "groove" one is in (Kirkham et al., 2003). Once in a "groove," even if it was a difficult one to settle into (because it required resisting a tendency to act otherwise, for example) it is not that difficult to continue along that path. It is re-mapping stimulus—response associations, changing mind- sets, that is quite difficult (Brass et al., 2003; Fagot 1994; Los, EFTA01098880 2040 M.C. Davidson et al. /Neumpsychologia 44 (2006)2037-2078 1996, 1999; Schuch & Koch, 2003, 2004; Wannk, Hommel, & Allport, 2003). We thus predicted that performance at all ages would be better in Incongruent -only blocks (where inhibition is consistently required on all trials) than in Mixed blocks (where inhibition is only required on the 50% of trials that are Incon- gruent), and that this difference would be greater the younger the children. This might seem obvious, but most studies of the classic Stroop effect still tend to administer the conditions in single-task blocks (read all the words or state the ink color of all the words), missing the most difficult condition (switching between having to read the words and having to state the ink color). A further seemingly independent finding that provides another example of the all or none principle is that it is eas- ier to switch everything, or nothing, than to switch one thing (e.g., the rule or the response) but not the other (Hommel et al., 2001; Kleinsorge, 1999; Meiran, 2000a,b; Rogers & Monsell, 1995; Schuch & Koch, 2004). Similarly, if you are supposed to press the color opposite to a stimulus it is easier to also press the button on the side opposite to the stimulus (rather than the typ- ical bias to respond on the same side as the stimulus; Hedge & Marsh, 1975). Issuing a global "change" or "opposite" command to all systems appears to be preferred by our neural machinery over a more selective command to just the action system or to just one aspect of cognition. This has been demonstrated not only in young adults, but also in older adults (Mayr, 2001) and children (Crone et al., in press). We predicted that we would demonstrate these effects, heretofore documented only in adults and older children, even in young children. Thus, we predicted that throughout our age span, participants would do better at switching tasks if the response-site also changed and would be slower and less accurate on switch trials when the response-site remained the same as on the previous trial. Another way of putting some of the above points is that con- text matters. For example, even "easy" trials do not seem so easy when they are presented in the context of switching between those and "harder trials. Knowing that sometimes you will have to switch can cause you to slow down (and perhaps err more) on trials where you do not have to switch. Local context matters; it matters what trials came before a particular trial. For example, was the rule on the preceding trial the same as on the current trial? Performance is better on nonswitch than on switch tri- als. Was the response-site on the preceding trial the same as on the current trial? Studies in adults have shown that performance is better on nonswitch, same-response -site trials than on non- switch, response-site-switch trials and on rule-switch, response- site-switch trials than on rule-switch, same-response -site trials. We predicted a different pattern in the youngest children and a more exaggerated version of the adult pattern in slightly older children (see above). Global context also matters; it matters what kind of trial block a given trial occurs in. Performance on the same type of trial (e.g., Congruent, Incongruent) in the same type of local con- text (e.g., nonswitch) varies depending on the larger context (e.g., a single-task block or Mixed block). Performance even on "easy" nonswitch trials (where the rule on the present trial is the same as on the previous trial) is usually slower and less accurate when they are presented in the context of having to periodically switch between rules than in a block of all nonswitch trials. Such global switch costs (the difference in performance on non- switch trials in a Mixed block versus in a single-task block; Fagot 1994, Mar, 2000) have been shown to be greater for elders than for younger adults (Kray, Eber, & Lindenberger, 2004; Kray & Lindenberger, 2000; Mayr, 2000; van Asselen & Ridderinkhof, 2000) and higher for children than for young adults (Cepeda et al., 2001; Cohen et al., 2001; Reimers & Maylor, 2005), though this has not been investigated in children as young as the youngest tested here and though some studies have not found an age difference in global switch costs (Crone et al., in press; Kray, Li, & Lindenberger, 2002). We predicted that global switch costs would not only be found in our youngest participants but would be more exaggerated the younger the child. Because of floor effects (subjects should already be slower and more error-prone in the Incongruent -only block), the effect of context (the Mixed block versus single-task block) should be greater on Congruent than Incongruent trials. We predicted that this would be more evident the younger the child. Thus, performance on "easy" (Congruent, nonswitch) trials should fall closer and closer to the level of "harder" trials in the context of sometimes having to switch back and forth the younger the child. 3. Methods 3.1. Participants A total of 325 individuals participated. ranging in age from 4 to 45 years. Of these. I 1 children were excluded from the analyses for failing to press any button or consistently pressing both. Of the remaining 314 participants. 50% were female (157 female. 157 male). Table 1 shows the number and gender of participants in each of the age groups. Children were recruited through local preschool and elementary school programs in the suburban Boston area. Adults Table 1 Number of participants within each age and gender group Age group' (years) Mean age (years) S.U. N Gender Female Male 4 4.43 0.25 30 14 16 5 5.19 0.17 30 14 16 6h 6.01 0.40 30 15 15 6h 6.22 0.35 30 12 IS 7 7.12 0.20 30 13 17 8 7.97 0.28 30 10 10 9 9.07 0.30 30 17 13 10 9.92 0.30 30 13 17 II 11.01 0.32 28 II 17 13 12.89 1.21 26 17 9 Adults 26.30 5.40 20 14 6 Total number of participants 314 157 157 4 The age groups were used for illustrative purposes when preparing graphs. All regression analyses used the actual ages of participants and treated age as a continuous variable. b TWo groups of 6-year-old children were tested to study the effects of short vs. long presentation time at this intermediate age. For one group. stimulus presentation time was 2501 ms. the slower version used with younger children. For the second group. stimulus presentation time was 750 nu, the faster version used with older children and adults. EFTA01098881 ACC. Davidson et al. /Neumpsychologia 44 (2006) 2037-2078 2011 were recruited from within the Eunice Kennedy Shrivcr Center in Waltham. MA. The majority of participants were Caucasian and from middle to upper middle class families. Informed consent was obtained from all adult participants and from a parent of each child participant: assent was obtained from the younger children and consent from the olderones. All participants received a small, token present for their participation. 3.2. Procedures common to all tests in our batten• All tasks were presented on a Macintosh computer using MacStim to present the stimuli and record responses. Participants held a button box (10cm x 14 cm x 3 cm) with both hands and used their thumbs to press the two response buttons. For each task a horizontal rectangle (6 cm x 18 cm) with a cen- tral fixation cross was presented on the computer screen (25cm x 33 cm). Only one stimulus was presented per trial and participants were positioned approxi- mately 50cm from the screen. Participants completed a set of four related tests designed to manipulate demands on working memory and inhibitor)• control (see Fig. I ). For adults and older children (>7 years). stimulus presentation time was 750ms. For younger children (4-6 years). stimulus presentation time was 2500ms. In all cases the interstimulus interval was 500 ms. resulting in total trial durations of 1250 and 3000 ms. respectively. An additional group of 6-year-oldchildren was tested with the short (adult) presentation time (750ms) to study the effects of presentation time at this intermediate age. Each task began with condition-specific instructions and a short practice block consisting of four or six trials. Different numbers of trials were used to allow presentation of all relevant trial types within each practice block. Partic- ipants could repeat the practice trials if needed to demonstrate learning of the requirements for a given task. Most children learned the task requirements with one practice block and no participant needed more than two practice blocks. The criterion for demonstrating learning was 75-80% correct on the practice trials and to be able to verbally tell the experimenter the rules. Testing blocks contained 20 trials and each participant completed 1 block for each condition of each task. except for the 2 conditions of the Abstract Shapes task. each of which contained 2 blocks (with a shoo break in between) for a total of 40 trials for each condition. The set of tests was administered with Arrows first. then Dots. Abstract Shapes (two then six shapes). and finally Pictures. A subset of participants were tested with Arrows presented last and Pictures presented first to check for order effects. but this did not affect performance. so results for both orders of presentation are collapsed together in the results reported here. 3.3. Procedures specifie le individual tests 3.3.1. Pictures This test is a classic Simon task. Here, a color picture of either a frog or butterfly was presented on the left or right side of the computer screen(see Fig. I). Each stimulus had an associated right or left response. The exact instructions given participants were: "If you sec a butterfly, press the button on the left. whether the butterfly appears on the left or right: if you see a frog. press the button on to the right. whether the frog appears on the left of right:' Small versions of the stimuli were attached next to the correct buttons on the response box to minimize the need to remember which stimulus was associated with which button. The stimuli were presented randomly on the left or right of the screen over the block of 20 trials, yielding Congruent (compatible) and Incongruent (incompatible) trials. 3.3.2. Arrows Here. a single large arrow was presented at the left or right of the computer screen. The arrow pointed either straight down (toward the response button on the same side as the arrow) or toward the opposite side at a 45' angle (toward the response button on the opposite side: see Fig. 0.0n Congruent trials. the arrow pointed straight down and participants were to respond on the same side as the arrow. On Incongruent trials. the arrow pointed diagonally toward the opposite side and participants were to respond on the side opposite the arrow. The precise instructions participants were told were. "1 want you to push the button the arrow is pointing toward. If the arrow is on the side of the box pointing down like this IE demonstrated] to this button. press this button. If the arrow is on the other side pointing down like this IE demonstrated] to this button. press this button. If the arrow is on this side. pointing down across the screen like this IE demonstrated] to this button. press this button. If the arrow is on the other side. pointing down across the screen like this IE demonstrated] to this button. press this button:' Congruent and Incongruent trials were presented in a randomized Mixed block of 20 trials. This requires inhibiting the tendency to respond on the same side as the stimulus when a diagonal arrow appears. but it requires little or no working memory. as the arrow points directly to the correct response button on all trials. 3.3.3. Dols The Dots test was designed to tax both working memory and inhibition. while the other tests were designed to tax primarily either working memory or inhibition, not both. Here, a large dot (diameter = 2_5 cm). was presented either at the left or right on each trial (sec Fig. I). Two types of Dots (striped or solid) were used. Striped Dots contained vertical black and white stripes. while solid Dots were a uniform gray color. These Dots were equated for visual characteristics such as size and luminance. For half of the participants a striped dot indicated they should make a response on the same side as the dot while a gray dot indicated they should respond on the side opposite the dot. These rules were reversed for the other half of the participants. An initial block of 20 Congruent trials (with all responses on the same side as the dot) was followed by a block of 20 Incongruent trials (with all responses on the side opposite the dot), and then by a Mixed block of 20 trials where Congruent and opposite trials were randomly intermixed. Instructions and practice were given before the Congruent and Incongruent blocks. Instructions alone were given before the Mixed block. e.g.. "Remember. gray same side: striped opposite: Memory is required on all trials of the Dots test to remember the rules (respond on the same or opposite side as the dot I. Inhibition is required on Incongruent trials to inhibit the prepotent response to respond on the same side as the visual stimulus. This task is similar to one used by Shaffer (1965) though there each subject received only one type of trial block (Congruent. Incongruent. or Mixed) and therefore subjects did not have the benefit of testing with the two easier trial blocks before receiving the Mixed block. The Dots task is also similar to a task used by Vu and Proctor (2004) but the rules for their single-task blocks did not refer to stimulus appearance and so the memory demand in their Mixed condition might have been greater than in ours. 3.3.4. Abstract Shapes In the Abstract Shapes test. unlike all other tests.each stimulus was presented in the center of the rectangle. Participants were taught a rule for each stimulus ("for this one press the left button": "for this one press right") during short prac- tice blocks before each testing condition. There were two conditions involving two- or six-Abstract-Shapes. Participants first completed the two-shapes condi- tion (2 blocks of 20 trials) and were then taught 4 additional rules. for a total of 6 shapes. and were then tested on another two blocks of 20 trials. The six- Abstract-Shapes condition taxes memory heavily (participants must hold six rules in mind). but it requires little or no inhibition (as the stimuli appear at the center of the screen and do not preferentially activate the right or left hand). 4. Results: general comments The three dependent measures were percentage of correct responses (accuracy), speed (reaction time MTH, and percent- age of anticipatory responses (AR). Linear regressions were used for all analyses involving age and each subject's exact age was entered, not simply the person's age grouping. Within-subject ANOVAs were used for analyses comparing tasks, conditions within task, or trial types. All binary comparisons included Tukey corrections for multiple comparisons. Whenever the vari- ance structure did not conform to the requirements for parametric analyses, logarithmic or arc sine transformations of the data were used to obtain the required conformity. All tables and figures present the raw, untransfonned data. A response time faster than 200 ms was considered antic- ipatory (too fast to be in response to the stimulus). Those EFTA01098882 2012 MC. Davidson et at /Neumpsychologia 44 (2006)2037-2078 Press Left Press Right CONGRUENT TRIALS INCONGRUENT TRIALS DOTS TEST: A SPATIAL INCOMPATIBILITY TASK with ARBITRARY STIMULI • Press Right • Press Left ARROWS TEST: A SPATIAL INCOMPATIBILITY TASK with ICONIC STIMULI Press -elf 4]Press Right Press Left Press Right PICTURES TEST: A SPATIAL INCOMPATIBILITY TASK that is a CLASSICAL SIMON TASK 4 Press Left Press Rignt MEMORY LOAD Low Medium High Low e Press Right 4 Press Left ABSTRACT SHAPES TEST: A MEMORY LOAD TASK Press Left Press Right Press Right Press Right Press Left Press Left INHIBITORY CONTROL DEMAND Medium High Dots-Congruent Dots-Incongruent. Pictures Arrows 2-Abstract -Shapes Dots-Mixed 6-Abstract -Shapes These 2 cells are logically possible. e.g . 6-Abstract Side (a 'Simon" task with 3 stimuli per response button) would be High Memory! Medium Inhib. However such tasks are too difficult Fig. I. Illustration of the tasks in our battery with a table summarizing the demands of each on memory and inhibition. EFTA01098883 M.C. Davidson et at. /Neuroptychologia 44 (2006)2037-2078 2043 responses were excluded from analyses of accuracy or speed, but were included in analyses of anticipatory responses (ARs). ARs occurred when a participant was either too eager and failed to wait for the stimulus on the current trial or failed to release the button following the previous trial. These anticipa- tory responses indicate inhibitory failures and are reported as a percentage of all possible responses where appropriate. A trial was considered correct if: (a) the first response following a stim- ulus was correct and (b) RT was >200 ms following stimulus onset. The percentage of correct responses was calculated by divid- ing the number of correct responses by the sum of correct plus incorrect responses. Anticipatory responses were excluded from that calculation. The median RI' for correct responses only was calculated for each participant. The median value, rather than the mean value, was used to reduce the effect of outlying RI's. The youngest children received a slower version of our tasks than the rest of the children and adults. The stimuli were pre- sented to the 4- and 5-year-olds and one group of 6-year-olds for much longer than they were presented to the rest of the children and adults (trial durations of 3000 and 1250 ms, respectively). Analyses over all ages might exaggerate RT differences over age (since children given longer to respond will naturally take longer) and might underestimate accuracy differences (since children given longer to respond are likely to make fewer errors). Hence, analyses of age differences are reported separately for the youngest children tested with a presentation time of 2500 ms and for all other participants tested with a presentation time of 750 ms. The effects of gender, and interactions of gender with age, were tested in all analyses. Significant effects were not found. Independent age-related regressions for male and female partic- ipants showed comparable R2 values across the three dependent measures for all tests. 5. Results: basic level results for the tasks that included an inhibitory component (Pictures, Arrows, and Dots) 5.1. Pictures The Pictures test was designed to provide a measure of the Simon effect in children. It tests the effect of an inhibitory demand (resisting the impulse to respond on the same side as the stimulus) with little or no working memory demand since small icons were attached above the appropriate response keys to indicate the correct response for each stimulus. The older the subjects, the better their performance (see Table 2). This was highly significant when all ages were included in the analyses (p <0.0001 for each of the three dependent variables) and for ages 6 years through adults tested with the brief presentation time (accuracy: F(1,222)= 17.93, p < 0.0001; RT: F(1,222) = 35.36, p <0.0001; anticipatory responses: F(1,222) = 10.8, p <0.001), the effect of age being particularly marked on speed of respond- ing. The youngest children (4-6 years of age) improved in speed and reduced anticipatory responses on the task over age, but given a long time to respond showed no difference over age in accuracy (RT: F(1,88)=4.58, p < 0.04; anticipatory responses: F(1,88) = 6.07, p <0.02). 5.2. Arrows The Arrows test was designed to require inhibitory control when a response was required on the side opposite the stimulus but to require little or no working memory as the stimuli them• selves point to the correct response button. Performance was better as a function of age, with increased accuracy, increased speed, and reduced anticipatory responses (Table 2). This was highly significant for accuracy and anticipatory responses when all ages were included in the analyses but not significant for speed of responding (accuracy: F(1,312)=57.06; p<0.0001; AR: F(1,312) = 35.73, p <0.0001). When the youngest children, tested with a long presentation time, were removed from the analyses, the age-related improvements in speed, as well as accu- racy and reduced incidence of anticipatory responses, were sig- nificant at p <0.0001 (F(1,222) = 76.88 [%correct]; 36.07 MTh 38.56 [AM). The youngest children (4-6 years of age) showed a steady reduction in anticipatory responses, and 6-year-olds responded correctly significantly more often than children of 4 or 5 years, but there was no difference over the age range of 4-6 years in response speed (accuracy: F( 1,88) = 10.69; p <0.005; AR: F(I ,88) = 6.5, p <0.02). 5.3. Dots In the Dots test there were three conditions (Congru- ent, Incongruent, and Mixed). Performance in each condition improved significantly as a function of age, with increased accu- racy and speed, and reduced anticipatory responses the older the participants (see Fig. 2). Unless othenvise noted, all results in the next three paragraphs for improvement over age are significant at p < 0.0001. For the Congruent condition, performance improved over age in the percentage of correct responses, RT. and reduced antici- patory responses (F(1,312) = 34.68. 116.97, and 8.42 (p < 0.05 for AR), respectively with all subjects in the analyses). The corresponding results for only those tested with the 750-ms stimulus presentation time (6-year-olds through adults) are F(1,222) = 14.33 (p < 0.001), 55.05, and 2.59 (NS for AR). The corresponding results for only those tested with the 2500-ms pre- sentation time (children of 4-6 years) are F(1,88) = 18.19 and 8.54 (p <0.005), and 18.52. For the Incongruent condition, with all subjects included, performance improved over age in accuracy (F(1,312)=46.60), speed (F(1,312) = 110.76), and reduced anticipatory responses (F(1,312)=39.77). The corresponding results for those ≥6 years of age are F(1,222)=33.09, 47.21, and 24.33. The corresponding results for those 4-6 years of age are F(1,88) = 7.76 (p < 0.005), <I (NS), and 15.07. For the Mixed condition, the results for improvement over age with all subjects included in the analyses are F(1,312)=66.65 (%correct), 62.15 (RT), and 42.84 (AR). For only those ≥6 years of age, the corresponding results are F(1,222)=61.95, 10.68, and 31.51. For only those 4-6 years of EFTA01098884 2044 MC. Davidson et at. /Neumpsychologia 44 (2006)2037-2078 Table 2 Table of means for each of the task conditions by age of the participants Task condition Age in years Average Tukey results 4 5 6 6 7 8 9 10 11 13 26 Accuracy (percentage of correct responses) Pictures 91.67 87.59 93.92 88.07 85.26 88.03 86.14 91.45 91.08 92.25 100.00 98.23 A Arrows 83.36 79.11 90.22 77.87 73.67 77.97 80.22 78.38 84.63 88.19 95.19 90.06 B Dots Congruent 96.33 94.96 98.61 96.00 96.86 99.65 99.30 99.67 99.62 99.55 98.50 91.47 B Incongruent 86.93 86.12 92.62 88.05 88.77 90.46 89.51 93.83 96.38 95.02 89.73 76.37 D Mixed 68.57 68.03 77.37 71.24 71.97 73.70 74.94 76.96 81.71 85.81 96.22 82.71 C Abstract Shapes Two-shapes 88.95 88.96 90.34 87.69 84.82 88.00 87.38 88.65 89.91 94.95 96.80 89.68 B Six-shapes 76.87 77.16 87.39 73.29 72.60 73.97 81.34 78.42 79.16 86.46 89.92 79.69 C Average 84.67 83.13 90.07 83.17 81.99 84.54 85.55 86.77 88.93 91.75 95.19 Reaction time (in ms) Pictures 1037.48 952.67 881.20 665.55 602.25 563.40 513.95 523.65 471.02 473.79 422.08 646.09 C Arrows 1121.28 1150.60 1090.42 797.73 725.57 683.07 613.12 651.77 578.04 555.46 465.25 766.57 BE Dots Congruent 775.37 684.58 677.37 474.53 412.12 395.05 356.87 341.13 331.46 323.87 271.30 458.51 A Incongruent 1023.12 905.75 875.02 619.87 546.27 501.63 444.02 451.83 398.09 402.87 321.28 589.98 CD Mixed 1172.32 1195.47 1177.00 787.10 728.18 725.98 644.72 654.15 597.36 593.85 562.98 803.55 E Abstract Shapes Two-shapes 892.80 853.88 795.17 608.15 552.03 520.58 478.38 463.13 436.23 434.56 371.40 582.39 D Six-shapes 1121.20 1038.10 987.53 726.72 694.15 662.98 640.55 61233 592.23 568.29 532.93 743.38 B Average 1020.51 968.72 926.24 668.52 608.65 578.96 527.37 528.31 486.35 478.95 421.03 Percentage of anticipatory responses Pictures 12.17 12.17 6.67 6.83 8.33 4.00 2.17 0.67 1.79 0.77 0.50 5.10 E Arrows 19.33 17.00 9.00 21.33 23.17 18.67 10.83 9.00 6.96 2.31 0.50 12.56 B Dots Congruent 13.83 10.67 2.67 6.33 7.17 6.83 5.50 6.83 6.25 5.38 2.75 6.75 A Incongruent 21.17 15.33 8.33 11.50 10.33 8.33 8.83 5.50 2.68 3.85 0.25 8.74 A Mixed 28.67 21.00 15.00 23.00 25.50 26.67 16.17 11.33 5.18 4.42 3.50 16.40 D Abstract Shapes Two-shapes 18.00 11.50 7.75 8.42 7.08 6.58 3.67 4.42 2.50 1.35 0.88 6.56 A E Six-shapes 18.00 17.83 11.58 15.33 15.33 13.83 6.08 5.83 4.73 2.98 2.75 10.39 B C Average 18.74 15.07 8.71 13.25 13.85 12.13 7.61 6.23 4.30 3.01 1.59 age, the corresponding results are F(1,88)= 6.24 (p< 0.05), <1 (NS), and 11.21 (p< 0.005). When the stimuli were presented for only 750 ms, 6-year-olds performed at a level of accuracy roughly comparable to that of 4-5-year-old children shown each stimulus for 2500 ms. While children of 4 or 5 years could perform well in the single-task blocks, even the Incongruent one, their average accuracy dipped below 70% in the Mixed block, even on Congruent trials. At the fast stimulus presentation rate (750ms), it was not until the age of II years that children began responding at >80% correct on average in the Mixed block. Even our oldest children (13 years old) were not yet correct on 90% of the items in the Mixed block. 6. Results: spatial compatibility effects 6.1. Spatial compatibility effects: Pictures task The Pictures test contained two intermixed trial types. Con- gruent and Incongruent, with spatial incompatibility present on the Incongruent trials. Participants made fewer errors and responded faster on Congruent than Incongruent trials (0[313[=10.1 [accuracy], 8.38 [RTI, both p< 0.0001; antici- patory responses NS; see Fig. 3). These comparisons indicate that the presence of spatial incompatibility affected perfor-mance. This effect was present at all ages and particularly pronounced in the younger children (t(89)=5.35 [accuracy], 4.49 IRT], both p<0.0001; ARs, NS). It was present, though smaller, in older children and adults 0(223) = 8.55 [accuracy[, 10.41 1RT1, both p <0.0001 ARs, NS) decreasing from the age of 6 years onward (accuracy: F(1,222)=7.46, p < 0.01; speed: F(1,222) = 5.23, p<0.02; see Fig. 3). Children of 4-6 years, allowed a long time to respond, showed no change in the absolute size of the effect over age. However taking into account their baseline speed on Congruent trials, the percent- age increase in RT on Incongruent trials decreased signifi- cantly over these ages (children 4-6 years old: t(89)=4.23, p <0.0001). Inhibition was required on only half the trials in the Pictures task (the Incongruent ones). Although children of 4-5 years were able to perform correctly on 90% of the Congruent trials, they were correct on only 80% of the Incongruent trials. Only the older subjects, and the 6-year-olds given a long time to respond, were able to perform at ≥85% on Incongruent trials in the Pic- tures task (88%, 88%, 89%, 94%, and 85%, at ages 10,11 and 13 years, young adult, and 6 years allowed a long time to respond, respectively). Accuracy at ages 6-9 years, given a short time to respond, was comparable to that seen at 4-5 years with the longer response window. EFTA01098885 M.C. Davidson et al. /Neap rhologia 44 (2006)2037-2078 Percent Correct (A) 100 90 80 70 60 1400 1200 11000 .5 800 iE 800 IS 400 cc ▪ 200 j8) 0 %Anticipatory Responses (C) 40 30 20 10 0 4 es • — •• • t• - t • a. 9 4 5 6 6 7 8 F. ▪ --a. 9 10 I & Congruent iincongnani I Mixed 13 20 • CI • • 6 StimuS presented for 2500 ms 6 7 8 9 10 11 Anticipatory Responses Errors 8 7 8 9 10 11 • 13 26 13 Stimuli presented for 750 ms Age In Years Fig. 2. Dots conditions: (A) accuracy. (B) reaction time and (C) anticipatory response errors. 6.2. Spatial compatibility effects: Arrows task The Arrows test also presented Congruent and Incongruent trials randomly intermixed. The youngest participants (4-6 years of age, tested with the 2500.ms presentation time) were both more accurate (4891=7.25. p <0.0001) and faster 01891=3.44, p <0.001) on Congruent than Incongruent trials (showing inter- ference similar to the Simon effect). Similarly, participants 6 years and older, tested with the 750-ms presentation time, were also more accurate and faster on Congruent than Incongru• ent trials (accuracy: 4223] = 8.76, p <0.0001; RT: 42231=7.91, p <0.0001). Among those ≥6 years, the difference in accuracy EFTA01098886 2046 MC. Davidson es at. /Neumps)rhologia 44 (2006)2037-2078 g ° 167 0 C • = E 0 o. c ,c E 25 o 2 O go 0 (A) 16 14 12 10 8 4 2 t 140 1) 6.• 6. 125 .S 80 O • ai 65 c (B) 36 25 31. CAGEy O• t 20 t-.• Th 1= 2 15 CC o ern • o 10 o ix o2a 3 cco €U 2 it (c) 5 0 4 5 6 6 7 B 9 10 11 f 4 10 I I 6 b 7 6 9 13 26 13 4 5 6 6 7 8 9 10 11 13 26 I Staub presented for 2500 ms Staub presented for 750 ms Age in Years Fig. 3. Simon effect on the Pictures task. (A) Difference in percent correct: Congruent minus Incongruent trials. (B)difference in reaction time: Incongruent minus Congruent trials and (C) percentage change in reaction time: (reaction time on Incongruent minus Congruent trials) divided by reaction time on Congruent trials. (but not speed) on Congruent versus Incongruent trials decreased as a function of age (accuracy: F(1,222) = 13.51, p <0.0003). 6.3. Spatial compatibility effects: Dots task There was a significant spatial incompatibility effect in the Mixed condition of the Dots task (where Congruent and Incon- gruent trials were again randomly intermixed). Participants were significantly faster on Congruent (spatially compatible) trials than on Incongruent (spatially incompatible) trials: $223) = 2.09, p < 0.04 (all subjects included); t(217)=2.49, p <0.01 (subjects ≥6 years old); NS for the youngest children. This effect of spatial incompatibility on speed did not change significantly over age. There was no significant effect of spatial incompatibility for accuracy or anticipatory responses on this task. 7. Discussion: compatibility effects Based on our hypothesis that even very young children can perform well when inhibition alone is taxed, we predicted they would perform well even on the Incongruent trials of EFTA01098887 ALC. Davidson a at. /Neuropsychologia 44 (2006)2037-2078 2047 the Pictures task, where memory demands were minimized. Since we hypothesiz