Anxiety disorders typically begin in childhood and adolescence and predict risk for many problems throughout life. Although some neuropsychological correlates have been described, more research is needed, particularly in adolescents. This study compares neurocognitive characteristics of anxious adolescents with and without comorbidity to externalizing disorders to those of typically developing comparison (TDC) adolescents and adolescents with externalizing disorders alone.
Methods:
The study included 57 adolescents 12–18 years of age (TDC, n=23; anxiety, n=16; externalizing, n=11; comorbid, n=7). We used a neuropsychological battery to assess eight domains: Orientation, attention, visual perception, memory, arithmetic, language, praxis, and executive function.
Results:
Multivariate analysis of variance revealed a main effect of group in the neurocognitive domains evaluated (F8,48=2.32, p=0.034, ηp2=0.279). Post-hoc analysis revealed that executive functions score differed among groups, specifically in the task of verbal fluency (F[df=3]=5.01, p=0.004, ηp2=0.221), with both the anxious groups (anxiety and comorbid) presenting a lower score than the TDC and externalizing groups. This effect was independent of age, intelligence, and levels of education.
Conclusions:
Verbal fluency is specifically impaired in adolescents with anxiety disorders. This extends results from neuroimaging research implicating prefrontal areas in pediatric anxiety disorder neurobiology, and has potential implications to new therapeutics.
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References
1.
AiraksinenE, LarssonM, ForsellY: Neuropsychological functions in anxiety disorders in population-based samples: evidence of episodic memory dysfunction. J Psychiatr Res, 39:207–214, 2005.
2.
BaldoJV, ShimamuraAP, DelisDC, KramerJ, KaplanE: Verbal and design fluency in patients with frontal lobe lesions. J Int Neuropsychol Soc, 7:586–596, 2001.
3.
BirnRM, KenworthyL, CaseL, CaravellaR, JonesTB, BandettiniPA, MartinA: Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage, 49:1099–1107, 2010.
4.
BlackfordJU, PineDS: Neural substrates of childhood anxiety disorders: A review of neuroimaging findings. Child Adolesc Psychiatr Clin N Am, 21:501–525, 2012.
5.
DellGS, SchwartzMF, MartinN, SaffranEM, GagnonDA: Lexical access in aphasic and nonaphasic speakers. Psychol Rev, 104:801–838, 1997.
6.
DeryM, ToupinJ, PauzeR, MercierH, FortinL: Neuropsychological characteristics of adolescents with conduct disorder: Association with attention-deficit-hyperactivity and aggression. J Abnorm Child Psychol, 27: 225–236, 1999.
7.
EkornasB, LundervoldAJ, TjusT, HeimannM: Anxiety disorders in 8-11-year-old children: Motor skill performance and self-perception of competence. Scand J Psychol, 51:271–277, 2010.
8.
FonsecaRP, SallesJFD, ParenteMA, de SallesJF, FonsecaRP: Development and content validity of the Brazilian Brief Neuropsychological Assessment Battery NEUPSILIN. Psychol Neurosci, 1:55–62, 2008.
9.
FonsecaRP, SallesJF, ParenteMA: Instrumento de Avaliação Neuropsicológica Breve NEUPSILIN. São Paulo: Vetor Editora; 2009.
10.
FrostLA, MoffittTE, McGeeR: Neuropsychological function and psychopathology in an unselected cohort of young adolescents. J Abnorm Psychol, 98: 307–313, 1989.
11.
GuntherT, HoltkampK, JollesJ, Herpertz–DahlmannB, KonradK: Verbal memory and aspects of attentional control in children and adolescents with anxiety disorders or depressive disorders. J Affect Disord, 82: 265–269, 2004.
12.
GuyW: ECDEU Assessment Manual for Psychopharmacology —Revised. Rockville, MD: 1976.
13.
HeckV, YatesD, PoggereL, TosiS, BandeiraD, TrentiniC: Validação dos subtestes verbais da versão de adaptação da WASI. [Validation of the Verbal Subtests from WASI Adapted Version.]. Aval Psicol, 8:33–42, 2009.
14.
HenryJD, CrawfordJR: A meta-analytic review of verbal fluency performance following focal cortical lesions. Neuropsychology, 18:284–295, 2004.
15.
KaufmanJ, BirmaherB, BrentD, RaoU, FlynnC, MoreciP, WilliamsonD, RyanN: Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): Initial reliability and validity data. J Am Acad Child Adolesc Psychiatry, 36: 980–988, 1997.
KristensenCH, GomesCFAG, JustoAR, VieiraK: Brazilian norms for the affective norms for English words. Trends Psychiatry Psychother, 33: 13–146, 2011.
18.
LeveltWJ, RoelofsA, MeyerAS: A theory of lexical access in speech production. Behav Brain Sci, 22:1–75, 1999.
19.
LissekS: Toward an account of clinical anxiety predicated on basic, neurally mapped mechanisms of Pavlovian fear-learning: The case for conditioned overgeneralization. Depress Anxiety, 29: 257–263, 2012.
20.
MerikangasKR, HeJP, BursteinM, SwansonSA, AvenevoliS, CuiL, BenjetC, GeorgiadesK, SwendsenJ: Lifetime prevalence of mental disorders in U.S. adolescents: results from the National Comorbidity Survey Replication—Adolescent Supplement (NCS-A). J Am Acad Child Adolesc Psychiatry, 49: 980–989, 2012.
21.
MiccoJA, HeninA, BiedermanJ, RosenbaumJF, PettyC, RindlaubLA, MurphyM, Hirshfeld–BeckerDR: Executive functioning in offspring at risk for depression and anxiety. Depress Anxiety, 26: 780–790, 2009.
MonkCS, KleinRG, TelzerEH, SchrothEA, MannuzzaS, MoultonJL3rd, GuardinoM, MastenCL, McClure–ToneEB, FrommS, BlairRJ, PineDS, ErnstM: Amygdala and nucleus accumbens activation to emotional facial expressions in children and adolescents at risk for major depression. Am J Psychiatry, 165:90–98, 2008a.
24.
MonkCS, TelzerEH, MoggK, BradleyBP, MaiX, LouroHM, ChenG, McClure–ToneEB, ErnstM, PineDS: Amygdala and ventrolateral prefrontal cortex activation to masked angry faces in children and adolescents with generalized anxiety disorder. Arch Gen Psychiatry, 65: 568–576, 2008b.
25.
NelsonBD, SarapasC, Robison–AndrewEJ, AltmanSE, CampbellML, ShankmanSA: Frontal brain asymmetry in depression with comorbid anxiety: A neuropsychological investigation. J Abnorm Psychol, 121:579–591, 2012.
26.
NicholsSL, WaschbuschDA: A review of the validity of laboratory cognitive tasks used to assess symptoms of ADHD. Child Psychiatry Hum Dev, 34: 297–315, 2004.
27.
NishimuraY, TaniiH, HaraN, InoueK, KaiyaH, NishidaA, OkadaM, OkazakiY: Relationship between the prefrontal function during a cognitive task and the severity of the symptoms in patients with panic disorder: A multi-channel NIRS study. Psychiatry Res, 172: 168–172, 2009.
28.
OhtaH, YamagataB, TomiokaH, TakahashiT, YanoM, NakagomeK, MimuraM: Hypofrontality in panic disorder and major depressive disorder assessed by multi-channel near-infrared spectroscopy. Depress Anxiety, 25: 1053–1059, 2008.
29.
PawlowskiJ, FonsecaRP, SallesJF, Pimenta ParenteMAM, BandeiraDR: Evidências de validade do Instrumento de Avaliação Neuropsicológica Breve NEUPSILIN. [Evidence of validity of the Neupsilin Brief Neuropsychological Assessment Instrument.]. ABP, 60:101–116, 2008.
30.
PawlowskiJ, RemorE, ParenteMAP, SallesJF, FonsecaRP, BandeiraDR: The influence of reading and writing habits associated with education on the neuropsychological performance of Brazilian adults. Read Writ, 25:2275–2289, 2012.
31.
Pearsall–JonesJG, PiekJP, RigoliD, MartinNC, LevyF: Motor disorder and anxious and depressive symptomatology: a monozygotic co-twin control approach. Res Dev Disabil, 32:1245–1252, 2011.
32.
PineDS: Research review: A neuroscience framework for pediatric anxiety disorders. J Child Psychol Psychiatry, 48:631–648, 2007.
33.
PineDS, HelfinsteinSM, Bar-HaimY, NelsonE, FoxNA: Challenges in developing novel treatments for childhood disorders: Lessons from research on anxiety. Neuropsychopharmacology, 34:213–228, 2009.
34.
PineDS, WassermanGA, WorkmanSB: Memory and anxiety in prepubertal boys at risk for delinquency. J Am Acad Child Adolesc Psychiatry, 38: 1024–1031, 1999.
35.
RivaD, NichelliF, DevotiM: Developmental aspects of verbal fluency and confrontation naming in children. Brain Lang, 71:267–284, 2000.
36.
RizzuttiS, SinnesEG, ScaramuzzaLF, FreitasL, PinheiroD, PalmaSM, MelloCB, MirandaMC, BuenoOF, MuszkatM.Clinical and neuropsychological profile in a sample of children with attention deficit hyperactivity disorders. Arq Neuropsiquiatr, 66:821–827, 2008.
37.
RodriguesAB, YamashitaÉT, ChiappettaALDML: Teste de fluência verbal no adulto e no idoso: verificação da aprendizagem verbal. [Verbal fluency test in adult and elderly: Verification of verbal learning.]. Rev CEFAC, 10:443–451, 2008.
38.
Rodriguez–ArandaC, MartinussenM: Age-related differences in performance of phonemic verbal fluency measured by Controlled Oral Word Association Task (COWAT): a meta-analytic study. Dev Neuropsychol, 30:697–717, 2006.
39.
SalumGA, IsolanLR, BosaVL, TocchettoAG, TecheSP, SchuchI, CostaJR, Costa MdeA, JarrosRB, MansurMA, KnijnikD, SilvaEA, KielingC, OliveiraMH, MedeirosE, BortoluzziA, ToazzaR, BlayaC, Leistner–SegalS, SallesJF, SilveiraPP, GoldaniMZ, HeldtE, ManfroGG: The multidimensional evaluation and treatment of anxiety in children and adolescents: Rationale, design, methods and preliminary findings. Rev Bras Psiquiatr, 33:181–195, 2011.
40.
SalumGA, MoggK, BradleyBP, GadelhaA, PanP, TamanahaAC, MoriyamaT, Graeff–MartinsAS, JarrosRB, PolanczykG, do RosarioMC, LeibenluftE, RohdeLA, ManfroGG, PineDS: Threat bias in attention orienting: Evidence of specificity in a large community-based study. Psychol Med, 1–13, 2012.
41.
SauzeonH, LestageP, RaboutetC, N'KaouaB, ClaverieB: Verbal fluency output in children aged 7–16 as a function of the production criterion: Qualitative analysis of clustering, switching processes, and semantic network exploitation. Brain Lang, 89:192–202, 2004.
42.
SchuerholzLJ, SingerHS, DencklaMB: Gender study of neuropsychological and neuromotor function in children with Tourette syndrome with and without attention-deficit hyperactivity disorder. J Child Neurol, 13:277–282, 1998.
43.
ShechnerT, BrittonJC, Perez–EdgarK, Bar–HaimY, ErnstM, FoxNA, LeibenluftE, PineDS: Attention biases, anxiety, and development: Toward or away from threats or rewards?. Depress Anxiety, 29:282–294, 2011.
44.
SnyderHR, HutchisonN, NyhusE, CurranT, BanichMT, O'ReillyRC, MunakataY:Neural inhibition enables selection during language processing. Proc Natl Acad Sci U S A, 107:16,483–16,488, 2010.
45.
StefanatosGA, BaronIS: Attention-deficit/hyperactivity disorder: A neuropsychological perspective towards DSM-V. Neuropsychol Rev, 17:5–38, 2007.
46.
StraussE, ShermanE, & SpreenO. A compendium of neuropsychological test: Administration, norms and commentary. New York: Oxford University Press; 2001.
47.
SutinAR, TerraccianoA, Kitner–TrioloMH, UdaM, SchlessingerD, ZondermanAB: Personality traits prospectively predict verbal fluency in a lifespan sample. Psychol Aging, 26:994–999, 2011.
TombaughTN, KozakJ, ReesL: Normative data stratified by age and education for two measures of verbal fluency: FAS and animal naming. Arch Clin Neuropsychol, 14:167–177, 1999.
50.
TorenP, SadehM, WolmerL, EldarS, KorenS, WeizmanR, LaorN: Neurocognitive correlates of anxiety disorders in children: A preliminary report. J Anxiety Disord, 14: 239–247, 2000.
51.
TroyerAK: Normative data for clustering and switching on verbal fluency tasks. J Clin Exp Neuropsychol, 22: 370–378, 2000.
52.
TroyerAK, MoscovitchM, WinocurG: Clustering and switching as two components of verbal fluency: Evidence from younger and older healthy adults. Neuropsychology, 11: 138–146, 1997.
53.
TupakSV, BadewienM, DreslerT, HahnT, ErnstLH, HerrmannMJ, FallgatterAJ, EhlisAC: Differential prefrontal and frontotemporal oxygenation patterns during phonemic and semantic verbal fluency. Neuropsychologia, 50:1565–1569, 2010.
54.
TurnerMA. Generating novel ideas: Fluency performance in high-functioning and learning disabled individuals with autism. J Child Psychol Psychiatry, 40:189–201, 1999.
55.
VasaRA, Roberson–NayR, KleinRG, MannuzzaS, MoultonJL3rd, GuardinoM, MerikangasA, CarlinoAR, PineDS: Memory deficits in children with and at risk for anxiety disorders. Depress Anxiety, 24:85–94, 2007.
56.
WechslerD: Wechsler Intelligence Scale for Children–Third edition (WISC-III): Manual. San Antonio: Psychological Corporation; 1991.
57.
YatesD, TrentiniC, TosiS, CorrêaS, PoggereL, ValliF: Apresentação da escala de inteligência wechsler abreviada (WASI). [Presentation of the Wechsler Intelligence Scale Short (WASI).]. Aval Psicol, 5:225–233, 2006.
58.
ZibettiMR, GindriG, PawlowskiJ, SallesJF, PMAMP., BandeiraDR, FachelJMG, FonsecaRP. Estudo comparativo de funções neuropsicológicas entre grupos etários de 21 a 90 anos. [Comparative study of neuropsychological functions among groups ages 21–90 years.]. Comp Gen Pharmacol, 2: 55–67, 2010.
