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Psychological Reports: Disability & Trauma 2012, 111, 2, 652-668. © Psychological Reports 2012

DOI 10.2466/15.10.19.PR0.111.5.652-668 ISSN 0033-2941

BraiN actiVity iN aDhD PatieNts PerForMiNg the coUNtiNg strooP tasK: a social NeUroscieNce aPProach1, 2

roBerto e. MercaDillo

Institute of Neurobiology Universidad Nacional Autónoma de México

celia trUJillo aND JUliÁN sÁNcheZ-cortaZar

Hospital Ángeles Metropolitano

FerNaNDo a. Barrios

Institute of Neurobiology, Universidad Nacional Autónoma de México

Summary.—Attention Deficit/Hyperactivity Disorder (ADHD) symptoms are manifested in social dynamics. in this study, the brain activity of eight child and adolescent patients diagnosed with aDhD was examined while they performed the counting stroop task and results were interpreted using social neuroscience premises. Brain activity was identified in frontal, parietal, and temporal regions related to the orienting system of attention and with linguistic, facial recognition, and mnemonic processes. consistent with previous reports, these patients showed no activation in prefrontal and anterior cingulate cortices related to the executive system of attention. also, they manifested activation in the insular cortex involving interoceptive processes that may be associated with impulsiveness. global brain activity involves a network formed during early development and includes experi- ential components such as learning of rules, reward systems, empathy, and decision making. an integrative assessment of aDhD should consider psychosocial and neurobiological causes integrated into an individual’s own experiences assembled throughout life.

Attention Deficit/Hyperactivity Disorder (ADHD) refers to diffi- culties in attention, inhibiting motor behavior, and behavioral and cog- nitive impulsiveness that can be diagnosed as a predominantly inatten- tive type, a predominantly hyperactive-impulsive type, and a combined type (american Psychiatric association, 2001). teenagers diagnosed with aDhD manifest a low performance in visual-motor capabilities (allen & Decker, 2008) as well as in several subscales of the Wechsler intelligence Scale, but their global coefficient could be within the normal range and no differences in cognitive skills have been reported between healthy partici- pants and those with aDhD (snow & sapp, 2000; galindo, De la Peña, De la rosa, robles, salvador, & cortés, 2001; Filippatou & livaniou, 2005). 1address correspondence to Dr. Fernando a. Barrios, institute of Neurobiology, Universidad Nacional autónoma de México, campus UNaM Juriquilla, Blvd. Juriquilla 3001, Querétaro, Qro, 76230, Mexico or e-mail ([email protected]). 2the authors appreciate the collaboration of the group working in the resonance Magnetic Unit of the hospital Ángeles Metropolitano, particularly Dr. angel sánchez-rey and tulio césar haro. We also thank leopoldo gonzález-santos, institute of Neurobiology, UNaM, for technical support in designing the brain images presented here and Paulina Barrios- giordano and Dorothy Pless for revising the manuscript. Finally, we thank the children, the adolescents, and their parents who agreed to participate in this study.

ADHD AnD SociAl neuroScience 653

aDhD dimensions correlate with both executive dysfunctions dependent on the frontal region and with impulsiveness associated with deficien- cies in working memory and alterations in the dorsolateral prefrontal cor- tex (gansler, lee, emerton, D’amato, Bhadelia, Jerram, et al., 2011). these atypical dimensions are regularly accompanied by emotional and learn- ing disorders, as well as by the Oppositional Defiant Disorder; the latter disorder is related with refusal to comply with rules and with aggressive behavior (Neef, Marckel, Ferreri, Bicard, endo, aman, et al., 2005; connor & Doerfler, 2008; Goodman, Gerstadt, Pfeffer, Stroh, & Valdez, 2008).

Morphometric studies have correlated aDhD with thinning of brain grey matter in the frontal, temporal, and parietal cortices (Valera, Fara- one, Murray, & seidman, 2007; shaw, lalonde, lepage, rabin, eckstrand, sharp, et al., 2009; almeida, ricardo-garcell, Prado, Barajas, Fernandez- Bouzas, avila, et al., 2010). controversially, structural alterations have been reported in several brain regions involving a variety of cognitive pro- cesses such as the corpus callosum, cingulate cortex, parahippocampal gyrus, basal ganglia, and cerebellum (Mackie, shaw, lenroot, Pierson, greenstein, Nugent, et al., 2007; Valera, et al., 2007; cao, cao, long, sun, sui, Zhu, et al., 2009).

at a functional level, studies applying functional Magnetic resonance imaging (fMri) have employed the stroop task, in which the participant must direct attention and impede automaticity, which is why it evaluates both selective attention and the inhibition of a dominant response, corre- sponding to both the attentive and the impulsive dimensions proposed for aDhD (Macleod, 2008). the counting version of the stroop task, ad- justed to the fMRI technique, has identified the anterior cingulate cortex and the dorsolateral prefrontal cortex as the fundamental brain regions in- volved in a healthy individual’s attention (Bush, Whalen, shin, & rauch, 2006). insular and striatal activation associated with impulsiveness is ob- served too (Bush, Frazier, rauch, seidman, Whalen, Jenike, et al., 1999; schneider, Krick, retz, hengesch, retz-Junginger, reith, et al., 2010). the striatal and insular activation, as well as the hypoactivation of the anteri- or cingulate and prefrontal cortices, suggest specific neurocognitive pro- cesses linked to different attentional dimensions and cognitive processes, rather than a generalized poor brain response, related with aDhD.

genetic data has related aDhD with inheritance and mutations af- fecting the transporter gene for dopamine, the neurotransmitter presented in the striatal-frontal reward system (casey, epstein, Buhle, liston, David- son, tonev, et al., 2007; langley, Fowler, grady, Moyzis, holmans, van den Bree, et al., 2009). in this sense, the pharmacological treatment with meth- ylphenidate improves the dopaminergic availability at the prefrontal level and reduces ADHD symptoms, although it is controversial how the effect

R. E. MERcadillo, et al.654

influences some related process such as mnemonic skills and verbal and nonverbal learning (gonzález-garrido, Barrios, de la serna-tuya, cocu- la-león, & gomez-Velazquez, 2009; Prehn-Kristensen, Krauel, hinrichs, Fischer, Malecki, schuetze, et al., 2011). thus, the reward and motor plan- ning systems are crucial for the cognitive and motivational comprehen- sion of aDhD, particularly in its impulsive aspects and long-term goal planning (luman, tripp, & scheres, 2010).

on the other hand, some proposals have associated the impulsiveness in ADHD with external causes affecting emotions. For example, a family environment with intrusive and rigid upbringing styles may result in chil- dren who are socially rejected because of their disruptive, aggressive, or antisocial behaviors. These situations are often accompanied by difficul- ties in interpreting the behavior of others, recognizing social problems, and generating efficient solutions, because these children tend to behave in the same way without regard to circumstances (goodman, et al., 2008; Pardos, Fernandez-Jaen, & Fernandez-Mayoralas, 2009).

The findings obtained through neuroimaging techniques, combined with biological and environmental data imply that neurocognitive sys- tems of attention are involved in social information processing. in this sense, it is necessary to integrate motivational mechanisms operating in ADHD that may influence interpersonal dynamics that allow interactions with the social world. this focus proposed by social neuroscience has sig- naled that social cognition begins with one’s own motor representation, as well as that of others and includes empathy as a skill required for per- sonal interrelation and inhibition. also intervening are homeostatic pro- cesses linked to basic emotions and motor and visceral reactions, and to controlled processes involved in decision making, motor control, affec- tive values, and the learning of semantic categories and norms. in addi- tion, the reward system is essential for mediating behaviors related to the satisfaction of one’s own needs and those of others and to norm learning (todorov, harris, & Fiske, 2006; adolphs, 2008).

the objective of this work was to evaluate the brain activity correlated with the performance of the counting stroop task in a child and teenage sample diagnosed with aDhD. it was hypothesized that brain activation will involve neurocognitive processes that can be interpreted within the framework of social neuroscience.

method Participants

a group of children and teenagers between 9 and 15 years old were in- vited to participate. all of the participants were mestizos with parents and grandparents who were born in Mexico, which has no predominant histo- ry of a minor ethnic group present in the country such as Pure indigenous,

ADHD AnD SociAl neuroScience 655

Jewish, or african-Mexican. their parents and/or their school authorities had identified behaviors and/or symptoms associated with ADHD, and they were diagnosed by neuropsychiatric evaluations based on DSM–IV diagnostic criteria. the international Neuropsychiatric interview for chil- dren and adolescents (M.i.N.i. KiD) and a subsequent neuropsychiatric evaluation confirmed the ADHD symptoms and identified symptoms re- lated to other psychiatric disorders. Before their participation, each child and his or her parents were informed of the details of the process and the objectives of the study. informed consent was given by the parent or legal guardian in consensus with the children’s acceptance. As verified by the personnel participating in the research, children who manifested a lack of interest and cooperation or were afraid to participate were excluded from the study without any consequence to their medical treatment carried out in the hospital. Medical research personnel accompanied the child and his or her parents during the process. all participants were strongly right- handed as measured by the edinburgh handedness inventory and none were taking any medication since one week before the study. the protocol was designed according the ethical principles suggested by the american Psychological association (2002), the helsinki Declaration, and the ethi- cal code for Psychologists in Mexico (sociedad Mexicana de Psicología, 2009). approval for this study was given by the research and teaching committees in the hospital Ángeles Metropolitano which examines the bioethics issues in any investigation proposed by universities and schools at the hospital units.

Patients were excluded when they manifested symptoms or disorders implying limited global cognitive faculties such as: Pervasive Develop- mental Disorder, literacy alterations, or perceptual and sensory problems. Patients were also excluded if their high-resolution fMri images showed radiological brain anomalies.

a version of the Wechsler intelligence scale, revised in Mexico, was applied in order to select those patients with a global iQ near the national average. after the selection process, a total sample of eight patients were recruited for the study. the general characteristics of the participants and relevant observations about their behavior and situations are shown in table 1. Cognitive Task and Behavioral Analysis

Using the e-prime software (e-Prime Psychology software tools, inc. Pittsburgh, Pa), a spanish version validated in Mexico of the counting stroop task was implemented (Mercadillo, sánchez-rey, sánchez-corta- zar, ramírez, & Barrios, 2011). in order to verify their complete compre- hension, the participants practiced the task on a laptop computer a week before the functional scanning. For the acquisition of functional images

R. E. MERcadillo, et al.656

taBle 1 basiC CharaCteristiCs of the eight Patients and relevant observations

Patient gender age aDhD Diagnosis

relevant Notes

1 F 9 combined type

she was referred by her parents, who reported in- attention and frequent daily task forgetfulness. at school a lack of concentration was reported while she performed exams and difficulties in learning english, geography, and mathematics. her academic performance this last year ranged from low to good. She has suffered bullying at school. her parents mentioned that she showed signs of depression in earlier months, but they were not observed in the present psychiatric evaluation. a maternal uncle presents aDhD. she was being treated with atomoxetine (strat- tera, 40 mg) before the present study. her family manifested a non-conflict interaction and par- ents cooperate in the therapy.

2 M 10 Predominantly inattentive

he was referred by the school, where teachers re- ported constant distraction. his academic per- formance this last year was from regular to good. he manifested a low tolerance to frus- tration. his parents reporedt bad behavior at home, non-fulfillment of chores, and hostility, particularly toward his brother. he was being treated with methylphenidate (Metadate, 20mg) before the study. his family manifested a non- conflict interaction and parents cooperated in the therapy.

3 M 11 Predominantly inattentive

he came to the appointment with his mother, who reported inattention and distraction at home. his academic performance was regular but manifested difficulties in understanding some topics related with mathematics and to maintain concentration while reading. he was not taking any medication before the study. he lived alone with his mother and any other relative was not included in his nuclear family. any relation with his parent is mentioned.

4 M 11 combined type

he came to the appointment through parent and school referral. he manifested some signs of anxiety, although without any evident psychi- atric diagnostic criteria. he presented an impul- sive, verbose, and aggressive profile, as well as low self-esteem and criteria that fulfill the Op- positional Defiant Disorder. His academic per- formance is good. he was being treated with atomoxetine (strattera, 60 mg) before the study. He was in psychotherapy due to conflicts re- lated with his parent’s divorce. his family mani- fested a non-conflict interaction and parents co- operated in the therapy.

(continued on next page)

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taBle 1 (Cont’d) basiC CharaCteristiCs of the eight Patients and relevant observations

Patient gender age aDhD Diagnosis

relevant Notes

5 M 13 Predominantly inattentive

he came to the appointment through parent and school referral where there were reported diffi- culties in academic performance, social adapta- tion, and aggressivness. he manifested symp- toms related with depressive disorder. he was being treated with atomoxetine (strattera, 40 mg). the aggressive behavior manifested by the patient has elicited troubled relations among the members of the family.

6 M 14 Predominantly inattentive

he came to the appointment through parent and school referral where they reported episodes of impulsiveness. he manifested an irritating conduct and symptoms of Oppositional Defi- ant Disorder. his academic performance was good. his father and paternal uncles presented aDhD. he was being treated with methylphe- nidate (concerta, 54 mg) before the study. Both the family and the school environments were described as extremely rigid.

7 M 14 Predominant- ly hyperac- tive/impul- sive

he came to the appointment through his parents’ referral. they reported impulsiveness and ag- gression problems within the family. he pres- ents criteria fulfilling Oppositional Defiant Dis- order. this conduct was not observed at school, where both interpersonal relations and academ- ic performance were reported to be adequate. he is a homozygotic twin, but his brother does not show symptoms linked to aDhD or any other behavioral or neurological disorder. he was being treated with risperidone (risperdal, .25 mg) and he was in gestalt therapy before the study. he lives with his father while his twin lives with his mother. Severe conflicts between the parents were presented.

8 M 15 combined type he came to the appointment through school refer- ral where bad behavior and failure to fulfill ba- sic norms was reported. his academic perfor- mance was low only in spanish, biology, and mathematics. he manifested signs of anxiety, authority rejection, and oppositional conduct, but made a constant effort to adapt to his school and family environment. any psychiatric symp- toms related with previous behaviors were identified in this study. Any pharmacological treatment was being taken before the study. an extremely rigid norm system in the school was presented.

R. E. MERcadillo, et al.658

Fig. 1. counting stroop task. the illustration represents the block design used and is an example of the test for both types of stimuli. the participants were informed that they would observe a series of blocks made up of 1 to 4 identical words on the screen in front of their eyes. the neutral blocks contained groups of words that named common animals (dog, cat, bird, or mouse). the interference blocks listed groups of words that were numbers (one, two, three, or four). The participants had to respond with their fingers, through a Lumina response system, with the number of words in each group. the lumina response system includes four buttons that are placed under the index and middle fingers of both hands. A number was assigned to each button and finger indicating the number of words presented on the screen. For the example illustrated in the figure, the correct response would be to press the button beneath the right middle finger, which indicates the number 4. The participants were informed that each group of words would change rapidly, which is why they had to re- spond immediately, but also attentively. After 30 sec. of fixation (F) on the red cross projected onto the screen, the block projection began and consisted of 20 trials (or groups of words) presented at 1500-msec. intervals. the task lasted 4 min. and alternated between a neutral block (N) and an interference block (I), each of which lasted 30 sec. Finally, the fixation cross was shown once again for 30 sec.

0 30 60 90 120 150

+ +

Neutral Trials Interference Trials

uno

perro

Time (sec.)

A new trial presented every 1,500 msec.

180 210 240 270 300

once in the scanner, the participants observed the task projected onto a white screen (110 × 70 cm), placed approximately 2 m away from their face, through the head coil mirror. the task presentation and participants’ responses were done with the lumina fMri manual response system (ce- drus corporation, san Pedro, ca), controlled by the e-Prime process. correct responses given for the neutral and for interference stimuli were analyzed by applying a non-parametric Mann-Whitney U test for inde- pendent samples. a detailed explanation of the task is shown in Fig. 1.

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Acquisition and Analysis of Functional Images the functional images were acquired using a general electric instru-

ment of 1.5 t in the Magnetic resonance Unit of the hospital Ángeles- Metropolitano in Mexico city. Following an fMri BolD protocol: rep- etition time (tr) = 3000, angular Displacement (Fa) 90, Field of Vision (FoV) = 24 cm, matrix 64 × 64 mm, 30 slices each 5 mm thick and zero sep- aration. the functional data were transferred to a workstation using the DicoM format and analyzed with sPM5 (Welcome Department of imag- ing Neuroscience, http://www.fil.ion.ucl.ac.uk/spm/).

the pre-statistical analysis of functional images included a temporary correction in order to synchronize the time differences between slices, re- alignment of the head movement, normalization in the standard MNi vol- ume (Montreal Neurological institute anatomical brain template), and smoothing (Friston, 2007). to estimate the average activation for all partic- ipants in the functional scanning while solving the counting stroop task, a second level statistical analysis was estimated with a one-sample t test using the first level contrast images of each participant. Contrasts between conditions (interference stimuli vs neutral stimuli) were obtained through a second level statistical analysis using sPM ( p ≤ .001). the MNi coordi- nates obtained from the sPM analysis were converted by the talairach De- amon Client system (Lancaster, Woldorff, Parsons, Liotti, Freitas, Rainey, et al., 2000) to obtain the brain region and the approximate Brodmann area.

results Behavioral data indicated significant differences between the correct

responses given for the neutral and for the interference stimuli (U16 = −3.36, p < .001; table 2). During the counting stroop task, all participants mani-

taBle 2 amount of CorreCt resPonses given by eaCh PartiCiPant for the 80 neutral

and 80 interferenCe stimuli during the exeCution of the Counting strooP task

Participant type of stimulus

Neutral (n = 80) interference (n = 80)

1 75 61 2 72 57 3 73 62 4 74 51 5 68 42 6 76 60 7 78 54 8 72 48

Note.—Significant differences were observed between the correct responses given for Neu- tral and interference stimuli (p < .001).

R. E. MERcadillo, et al.660

fested bilateral frontal activity in the premotor area (Brodmann area 6), and right lateralization in the frontal and the left prefrontal region, corre- sponding with Brodmann areas 8 and 9, respectively (Fig. 2).

Bilateral parietal activity was observed in the precuneus (Brodmann area 7), the superior temporal gyrus (Brodmann area 22; Figs. 2 and 3), as well as activity being observedin the right insular cortex, parahippocampal gyrus, and globus pallidus (Fig. 3, table 3).

disCussion Behavioral results agree with previous studies reporting that aDhD

patients manifest a worse performance during the interference condition than during the neutral condition while performing the stroop task (Bush, et al., 1999; Macleod, 2008; Mercadillo, et al., 2011).

the frontal activation in Brodmann areas 6, 8, and 9 and parietal ac- tivation in Brodmann area 7 identified in patients suggests a neurocog-

Fig. 2. average of functional results for all participants in surface-rendered views rep- resenting Brodmann areas in frontal (Brodmann areas 6, 8, and 9), parietal (Brodmann area 7), and temporal (Brodmann area 22) cortical activation while subjects executed the count- ing Stroop Task. Brain activations are significant at p = .001.

Frontal View

Lateral Right View

Dorsal View

BA 9 BA 6

BA 6

BA 8

BA 7

BA 22

BA 7

Lateral Left View

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nitive activity linked to the alerting and orientation systems comprising attention (Posner, sheese, odludas, & tang, 2006). the temporal activa- tion in Brodmann area 22 is correlated with linguistic functions while the motor regulation is inferred by the activation in the globus pallidus. Work- ing memory processes are represented in Brodmann area 9 and in the parahippocampal gyrus. this latter structure involves the mnemonic infor- mation necessary for social decision making (owen, McMillan, laird, & Bullmore, 2005; axmacher, schmitz, Weinreich, elger, & Fell, 2008). the cognitive function of these brain regions is also related to processes con-

Fig. 3. average of all participants’ functional maps. sagittal, coronal, and axial views representing the activation (blue cross line) in left Brodmann area 22 (a), right insular cortex (B), right parahippocampal gyrus (c), and right globus pallidus (D) while participants ex- ecuted the counting stroop task; p = .001.

20 18 16 14 12 10 8 6 4 2 0

R. E. MERcadillo, et al.662

cerning social cognition, such as empathy and recognition of human faces (hadjikhani, Joseph, snyder, & tager-Flusberg, 2006; Benuzzi, Pugnaghi, Meletti, Lui, Serafini, Baraldi, et al., 2007).

in healthy participants, the selective attention and inhibition process- es elicited by the stroop task performance engage the executive attention- al system regulated by activity in the prefrontal orbital and the anterior cingulate cortices (Bush, et al., 2006). an optimal analysis of the brain func- tion in patients diagnosed with aDhD correlated with the performance of a cognitive task requires a comparison with healthy or control samples in order to strengthen the results. this comparison was not presented in this study due to the ethical difficulties in Mexico to recruit a sample of healthy children who accept participation in an experimental investiga- tion when it is not necessary for the children’s health. Nevertheless, in keeping with previous reports of aDhD patients including samples of children (Bush, et al., 1999; Mercadillo, et al., 2011), the participants of this study showed no activity in the prefrontal orbital and the anterior cin- gulate cortices regulating selective attention and inhibition. the function of the anterior cingulate cortex is fundamental for decision making since it involves the exchange of semantic information with temporal regions (Brodmann area 22), with pre-motor areas involved in movement plan- ning (Brodmann areas 6 and 8), and with parietal regions related to sen- sory integration (Brodmann area 7) observed here (Koski & Paus, 2000; Posner, rothbart, sheese, & tang, 2007). the cognitive function of the pre- frontal orbital cortex has been linked to norm-abiding processes, recogni- tion of the self, decision making, and regulating impulsive behavior such

taBle 3 average of the aCtivated brain regions for all PartiCiPants identified by bold signal dur-

ing the exeCution of the Counting strooP task

Brain region laterality Ba cluster T MNi coordinates

x y z

Precuneus r 7 1,578 6.41 32 −58 36 Middle frontal gyrus r 6 653 5.86 24 0 62 Middle frontal gyrus r 8 620 4.17 38 32 36 Parahippocampal gyrus r 36 136 3.32 46 −38 −14 Globus pallidus r 131 3.45 16 0 −6 Insula r 13 26 2.80 40 22 6 Precentral gyrus l 6 7,916 8.28 −38 −2 26 Precuneus l 7 4,683 20.35 −16 −62 44 Superior temporal gyrus l 22 440 4.89 −56 −52 10 Medial frontal gyrus l 9 581 4.33 −24 44 18 Note.—Significant activation at p < 0.01. l = left, r = right, Ba = approximate Brodmann’s area location obtained by using the talairach Deamon client system. cluster is the size of the ac- tivated area in number of voxels.

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as anger and aggression (Nelson & trainor, 2007; adolphs, 2008). there- fore, the brain activity observed would imply alterations in the attention decision system but not in their primary processes.

in agreement with prior reports (Bush, et al., 1999; Mercadillo, et al., 2011), insular activation was observed in these participants. the activation of the insula while performing tasks eliciting inhibition implies an affer- ent evaluation of the body’s information, which allows the interoceptive representations to resolve conflicts considering the cost to the self and in making social decisions (craig, 2002; Brass & haggard, 2007). the insular activity in concert with the simultaneous lack of activity in the anterior cingulate and the prefrontal orbital cortices could be related to the impul- siveness manifested in aDhD as continuously uninhibited internal states associated with the participants’ sensation seeking, emotions, and hostile behavior (Martin, Kelly, rayens, Brogli, himelreich, Brenzel, et al., 2004; aarts & roelofs, 2011).

The Stroop task reveals forms or styles of flexible or rigid thought. Flexible thought implies the capacity to change quickly from one action to another, while rigidity refers to difficulty ignoring distractors and in- hibiting automatic responses. Participants with aDhD frequently present controversial attachment relations and manifest inflexible cognitive styles linked to rigid upbringing, intrusive family environments, or attachment issues, as was observed in some of the patients participating in this study (Niederhofer, 2009; Pardos, et al., 2009). the cognitive function of the ante- rior cingulate is correlated with inhibitory responses and styles culturally learned and its neural regulation of inhibition is influenced by ontogenet- ic processes (Booth, Burman, Meyer, lei, trommer, Davenport, et al., 2003; amodio, Jost, Master, & yee, 2007). the lack of prefrontal and cingulate activity could reflect learning or habits that reduce the inhibitory capabili- ties and elicit rigid decisions in the patients’ social interactions. also, this brain activity could be related to parents’ behaviors becoming more rigid as they attempt to control the expressions of aDhD in their children.

the absence of activity in the orbital and anterior cingulate cortices concomitant with activation of the insular cortex could reflect the learning of cognitive strategies in early stages of life. the genetic factors associat- ed with alterations in the dopaminergic system and in the function of the frontal cortex (Wohl, Boni, asch, cortese, orejarena, Mouren, et al., 2008), in conjunction with the cognitive rigidity related to environmental and family factors, may not directly cause aDhD, but rather, they may form the internal and external environments in which this learning is assem- bled. this may explain the variability in the morphometric, environmen- tal, and social factors associated with aDhD.

the social cognition is partially regulated by parietal and frontal sys-

R. E. MERcadillo, et al.664

tems observed in the patients and required for the cognitive representa- tion of others actions and intentions, as well as memory and language. the activation of these brain regions may suppose an empathic factor as- sociated with aDhD and may be necessary for inferring the state of oth- er people and for inhibiting aggressive or impulsive behavior through self-control (Nelson & trainor, 2007; adolphs, 2008; iacoboni, 2009). the self-control of impulsiveness based on social and empathic processes is relevant due to the co-morbidity between ADHD, Oppositional Defiant Disorder, aggressive behaviors and suicidal tendencies that put at risk the lives of the patient and others (amen, Prunella, Fallon, amen & hanks, 2009; Connor & Doerfler, 2008; Goodman, et al., 2008).

the diversity in family relations, environmental circumstances and academic performance in aDhD patients, as observed in the sample of this study, may imply that the neurocognitive link between empathy and norm learning emphasizes the value of using multimodal treatments to help the child adapt to the environment. For example, medical treatment based on methylphenidate acts at the level of the dopaminergic prefron- tal and reward systems involved in one’s own welfare and that of others (rilling,gutman, Zeh, Pagnoni, Berns, & Kilts, 2002), and it would pro- mote a receptive state for norm learning associated with satisfactory ex- periences. as observed in previous studies, a pleasant motivational state associated with norms-learning in aDhD patients can be reached by non- pharmacological treatments, for example, given high incentives during cognitive performance (slusarek, Velling, Bunk & eggers, 2001).

considering learned impulsive and rigid thought styles in aDhD fa- vors the application of therapies based on resolving conflict and address- ing the motivational dimension involving the reward system at the meso- limbic and striatal level, and the executive processes concerning frontal functions and the anterior cingulated cortex (ison, 2001; sonuga-Barke, 2003). This last idea agrees with proposals suggesting that Attention Defi- cit/hyperactivity Disorder interferes with other executive functions such as working memory, and motivational and affective self-regulation (Bark- ley, 1997) which are involved in social interactions.

as mentioned in the hypothesis, the brain activity observed in the pa- tients involves neurocognitive processes that can be interpreted within the framework of social cognition. these interpretations are limited in several ways that must be overcome in future research: the small sample, difficul- ties recruiting participants without other psychiatric disorders, and the children’s refusal to participate. also, the lack of a control group must be considered as problematic, given the technical restrictions when analyz- ing the BolD signals in fMri. BolD does indicate the brain regions ac- tivated during the performance of the counting stroop task, but not the temporal sequence of these brain activations.

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even with the restrictions mentioned above, it is plausible to inter- pret the results with reference to an understanding of aDhD within social neuroscience. such an understanding implies that neural structural and functional factors collaborate within a developmental process involving the experience and internalization of family and cultural dynamics, which may or may not favor the adaptation of the individual to them (Shonkoff & Phillips, 2000; Conti, 2004; Timimi, Moncrieff, Jureidini, Leo, Cohen, Whitfield, et al., 2004). this view would lead to a search for bio-cultural patterns correlated with aDhD backed both by respondents’ experiential and neurobiological interactions.

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Accepted September 26, 2012.

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