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Estudios originales
Medwave 2015 Abr;15(3):e6112 doi: 10.5867/medwave.2015.03.6112
Estudio de asociación familiar entre las alteraciones de los potenciales evocados N200/P300 y el fenotipo clínico en familias cubanas con esquizofrenia paranoide
Evoked potentials N200/P300 disorders and clinical phenotype in Cuban families with paranoid schizophrenia: a family-based association study
Seidel Guerra López, Migdyrai Martín Reyes, María de los Ángeles Pedroso Rodríguez, Adnelys Reyes Berazain, Raúl Mendoza Quiñones, Tania Martha Bravo Collazo, Thais Días de Villarvilla, María Julia Machado Cano, María Antonieta Bobés León
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Palabras clave: evoked potentials N200; event-related potentials, P300; paranoid schizophrenia, endophenotype

Abstract

INTRODUCTION
N200 and P300 event-related evoked potentials provide sensitive measurements of sensory and cognitive function and have been used to study information processing in patients with schizophrenia and their unaffected first-degree relatives. Reduced amplitude and increased latency of N200 and P300 potentials have been consistently reported in schizophrenia. Thus, event-related evoked potentials abnormalities are promising possible biological markers for genetic vulnerability to schizophrenia.

OBJECTIVE
To assess the association of changes in latency, amplitude and topographic distribution of potentials N200 and P300 of patients with paranoid schizophrenia and their healthy first-degree relatives, in families with schizophrenia multiplex.

METHODOLOGY
We measured latency and amplitude of the N200 and P300 component of evoked potentials using an auditory odd-ball paradigm in 25 schizophrenic patients (probands) from 60 families multiply affected with paranoid schizophrenia, 23 of their non-schizophrenic first-degree relatives and 25 unrelated healthy controls, through a study of family association.

RESULTS
Schizophrenic patients and their relatives showed significant latency prolongation and amplitude reduction of the N200 and P300 waves compared to controls. Left-temporal as compared to right-temporal N200 and P300 were significantly smaller in schizophrenic patients and their non-schizophrenic first-degree relatives than in controls. Our results suggest that event-related evoked potentials abnormalities may serve as markers of genetic vulnerability in schizophrenia.

CONCLUSIONS
Confirming results of other researchers, this present study suggests that latency prolongation and amplitude reduction of the N200 and P300 waves and an altered topography at temporal sites may be a trait “marker” of paranoid schizophrenia.


 

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INTRODUCTION
N200 and P300 event-related evoked potentials provide sensitive measurements of sensory and cognitive function and have been used to study information processing in patients with schizophrenia and their unaffected first-degree relatives. Reduced amplitude and increased latency of N200 and P300 potentials have been consistently reported in schizophrenia. Thus, event-related evoked potentials abnormalities are promising possible biological markers for genetic vulnerability to schizophrenia.

OBJECTIVE
To assess the association of changes in latency, amplitude and topographic distribution of potentials N200 and P300 of patients with paranoid schizophrenia and their healthy first-degree relatives, in families with schizophrenia multiplex.

METHODOLOGY
We measured latency and amplitude of the N200 and P300 component of evoked potentials using an auditory odd-ball paradigm in 25 schizophrenic patients (probands) from 60 families multiply affected with paranoid schizophrenia, 23 of their non-schizophrenic first-degree relatives and 25 unrelated healthy controls, through a study of family association.

RESULTS
Schizophrenic patients and their relatives showed significant latency prolongation and amplitude reduction of the N200 and P300 waves compared to controls. Left-temporal as compared to right-temporal N200 and P300 were significantly smaller in schizophrenic patients and their non-schizophrenic first-degree relatives than in controls. Our results suggest that event-related evoked potentials abnormalities may serve as markers of genetic vulnerability in schizophrenia.

CONCLUSIONS
Confirming results of other researchers, this present study suggests that latency prolongation and amplitude reduction of the N200 and P300 waves and an altered topography at temporal sites may be a trait “marker” of paranoid schizophrenia.

Autores: Seidel Guerra López[1,2], Migdyrai Martín Reyes[3], María de los Ángeles Pedroso Rodríguez[4], Adnelys Reyes Berazain[5], Raúl Mendoza Quiñones[5], Tania Martha Bravo Collazo[6], Thais Días de Villarvilla[5], María Julia Machado Cano[7], María Antonieta Bobés León[5]

Filiación:
[1] Universidad Nacional del Este, Alto Paraná, Paraguay
[2] Universidad de Integración Latinoamericana, Foz de Iguazú, Paraná, Brasil
[3] Clínica de Rehabilitación de Salud Mental, Servicio Navarro de Salud, Pamplona, Navarra, España
[4] Centro de Investigaciones Médicas, Facultad de Ciencias de la Salud, Universidad Nacional del Este, Minga Guazú, Paraguay
[5] Departamento de Neurociencias de Cuba, Centro de Neurociencias de Cuba, La Habana, Cuba
[6] Centros de Investigación y Tratamiento de las Adicciones (CITA) Dosrius, Barcelona, España
[7] Universidad de Ciencias Médicas de Ciego de Ávila, Ciego de Ávila, Cuba

E-mail: seidelguerra@yahoo.es

Correspondencia a:
[1] Km. 16 Acaray
Avda. Mcal. López entre Mcal. Estigarribia y Padre Moleón
Minga Guazú
Paraguay

Citación: Guerra López S, Martín Reyes M, Pedroso Rodríguez MA, Reyes Berazain A, Mendoza Quiñones R, Bravo Collazo T, et al. Evoked potentials N200/P300 disorders and clinical phenotype in Cuban families with paranoid schizophrenia: a family-based association study. Medwave 2015 Abr;15(3):e6112 doi: 10.5867/medwave.2015.03.6112

Fecha de envío: 27/11/2014

Fecha de aceptación: 17/3/2015

Fecha de publicación: 1/4/2015

Origen: no solicitado

Tipo de revisión: con revisión por cinco pares revisores externos, a doble ciego

Ficha PubMed

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  1. Amenedo E, Díaz F. Aging-related changes in processing of non-target and target stimuli during an auditory oddball task. Biol Psychol. 1998 Aug;48(3):235-67. | PubMed |
  2. American Psychiatric Association. DSM-IV. Diagnostic and statistical manual of mental disorders, 4 ed, Washington, DC: American Psychiatric Association, 1994.
  3. Braff DL. Psychophysiological and information processing approaches to schizophrenia. En: Neurobiological foundation of mental illness. New York: Oxford University Press, 1999:258-271.
  4. Blackwood DH, Young AH, McQueen JK, Martin MJ, Roxborough HM, Muir WJ, et al. Magnetic resonance imaging in schizophrenia: altered brain morphology associated with P300 abnormalities and eye tracking dysfunction. Biol Psychiatry. 1991 Oct;30(8):753-69. | PubMed |
  5. Bharath S, Gangadhar BN, Janakiramaiah N. P300 in family studies of schizophrenia: review and critique. Int J Psychophysiol. 2000 Oct;38(1):43-54. | PubMed |
  6. Boutros N, Nasrallah H, Leighty R, Torello M, Tueting P, Olson S. Auditory evoked potentials in schizophrenia. Biol Psychiatry. 1996;39(7):651. | CrossRef |
  7. Bramon E, McDonald C, Croft RJ, Landau S, Filbey F, Gruzelier JH, et al. Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. Neuroimage. 2005 Oct 1;27(4):960-8. | PubMed |
  8. Brown KJ, Gonsalvez CJ, Harris AW, Williams LM, Gordon E. Target and non-target ERP disturbances in first episode vs. chronic schizophrenia. Clin Neurophysiol. 2002 Nov;113(11):1754-63. | CrossRef | PubMed |
  9. Cohen RA, Sparling-Cohen YA, O’Donnell BF. The Neuropsychology of Attention. New York: Plenum Press, 1993.
  10. Donchin E, Coles MGH. Is the P300 component a manifestation of context updating ? Behav Brain Sci. 1988;11(3):357-373. | CrossRef |
  11. Debruille JB, Schneider-Schmid A, Dann P, King S, Laporta M, Bicu M. The correlation between positive symptoms and left temporal event-related potentials in the P300 time window is auditory specific and training sensitive. Schizophr Res. 2005 Oct 15;78(2-3):117-25. | CrossRef | PubMed |
  12. Egan MF, Duncan CC, Suddath RL, Kirch DG, Mirsky AF, Wyatt RJ. Event-related potential abnormalities correlate with structural brain alterations and clinical features in patients with chronic schizophrenia. Schizophrenia Research. 1994;11(3):259-271. | CrossRef |
  13. Fabiani M, Gratton G, Karis D, Donchin E: Definition, identification, and reliability of measurement of the P300 component of the event-related brain potential. En: Advances in Psychophysiology, vol 2. Greenwich, CT: JAI Press, 1987.
  14. Ford JM, Mathalon DH, White PM, Pfefferbaum A. Left temporal deficit of P300 in patients with schizophrenia: effects of task. Int J Psychophysiol. 2000 Oct;38(1):71-9. | PubMed |
  15. Forte A, Bernardo A, Caputo F, Bucci P, Mucci A, Galderisi S, et al. P300 Brain Microstate in deficit and nondeficit schizophrenia. Eur Psychiatr. 2002;17(1):188. | PubMed |
  16. Frodl T, Meisenzahl EM, Müller D, Greiner J, Juckel G, Leinsinger G, et al. Corpus callosum and P300 in schizophrenia. Schizophr Res. 2001 Apr 15;49(1-2):107-19. | CrossRef | PubMed |
  17. Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003 Apr;160(4):636-45. | CrossRef | PubMed |
  18. Gonul AS, Suer C, Coburn K, Ozesmi C, Oguz A, Yilmaz A. Effects of olanzapine on auditory P300 in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2003 Feb;27(1):173-7. | PubMed |
  19. Grillon C, Courchesne E, Ameli R, Geyer MA, Braff DL. Increased distractibility in schizophrenic patients. Electrophysiologic and behavioral evidence. Arch Gen Psychiatry. 1990 Feb;47(2):171-9. | CrossRef | PubMed |
  20. Guerra S, Ibáñez A, Martín M, Bobes MA, Reyes A, Mendoza R, et al. N400 deficits from semantic matching of pictures in probands and first-degree relatives from multiplex schizophrenia families. Brain Cogn. 2009 Jul;70(2):221-30. | CrossRef | PubMed |
  21. Higashima M, Kawasaki Y, Urata K, Sakai N, Nagasawa T, Koshino Y, et al. Regional cerebral blood flow in male schizophrenic patients performing an auditory discrimination task. Schizophr Res. 2000 Mar 16;42(1):29-39. | CrossRef | PubMed |
  22. Shaikh M, Hall MH, Schulze K, Dutt A, Li K, Williams I, Walshe M, et al. Effect of DISC1 on the P300 waveform in psychosis. Schizophr Bull. 2013 Jan;39(1):161-7. | CrossRef | PubMed |
  23. Havermans R, Honig A, Vuurman EF, Krabbendam L, Wilmink J, Lamers T, et al. A controlled study of temporal lobe structure volumes and P300 responses in schizophrenic patients with persistent auditory hallucinations. Schizophr Res. 1999 Aug 17;38(2-3):151-8. | PubMed |
  24. Hotchkiss AP, Harvey PD. Effect of concurrent distraction on thought disorder in schizophrenia. American Journal of Psychiatry. 1990;147(2):153-156.
  25. Díaz-Anzaldúa A, Velázquez-Pérez J, Berlanga C. Endophenotypes and biomarkers: an approach to molecular genetic studies of mental disorders. Salud Mental 2013;36(3):161-168. | Link |
  26. Ogura C, Nageishi Y, Omura F, Fukao K, Ohta H, Kishimoto A, er al. N200 component of event-related potentials in depression. Biol Psychiatry. 1993 May 15;33(10):720-6. | CrossRef | PubMed |
  27. Meisenzahl EM, Frodl T, Müller D, Schmitt G, Gallinat J, Zetzsche T, et al. Superior temporal gyrus and P300 in schizophrenia: a combined ERP/structural magnetic resonance imaging investigation. J Psychiatr Res. 2004 Mar-Apr;38(2):153-62. | CrossRef | PubMed |
  28. McCarley RW, O’Donnell BF, Niznikiewicz MA, Salisbury DF, Potts GF, Hirayasu Y, et al. Update on electrophysiology in schizophrenia. Int Rev Psychiatry. 1997;9(4):373-386. | CrossRef |
  29. Matthysse S, Holzman PS, Lange K. The genetic transmission of schizophrenia: application of Mendelian latent structure analysis to eye tracking dysfunctions in schizophrenia and affective disorder. J Psychiatr Res. 1986;20(1):57-67. | PubMed |
  30. Moser RK, Cienfuegos A, Barros J, Javitt D. Auditory distraction and thought disorder in chronic schizophrenic inpatients. Evidence for separate contributions by incapacity and poor allocation and a subsyndrome related to the allocation deficit. Schizophr Res. 2001 Sep 1;51(2-3):163-70. | CrossRef | PubMed |
  31. Vázquez- Barquero JL, et al. Report on the Spanish Translation of the SCAN, Schedules and Glossary. Informe a la Organización Mundial de la Salud. Santander, España: Unidad de Investigación en Psiquiatría Social de Cantabria, 1992.
  32. Kay SR, Fiszbein A, Vital-Herne M, Fuentes LS. The Positive and Negative Syndrome Scale--Spanish adaptation. J Nerv Ment Dis. 1990 Aug;178(8):510-7. | PubMed |
  33. Bunney WE Jr, Hetrick WP, Bunney BG, Patterson JV, Jin Y, Potkin SG, Sandman CA. Structured Interview for Assessing Perceptual Anomalies (SIAPA). Schizophr Bull. 1999;25(3):577-92. | CrossRef | PubMed |
  34. Frangou S, Sharma T, Alarcon G, Sigmudsson T, Takei N, Binnie C, Murray RM. The Maudsley Family Study, II: Endogenous event-related potentials in familial schizophrenia. Schizophr Res. 1997 Jan 17;23(1):45-53. | CrossRef | PubMed |
  35. Schreiber H, Stolz-Born G, Rothmeier J, Kornhuber A, Kornhuber HH, Born J. Endogenous event-related brain potentials and psychometric performance in children at risk for schizophrenia. Biol Psychiatry. 1991 Jul 15;30(2):177-89. | CrossRef | PubMed |
  36. Surwillo WW. Cortical evoked potentials in monozygotic twins and unrelated subjects: comparisons of exogenous and endogenous components. Behav Genet. 1980 Mar;10(2):201-9. | PubMed |
  37. Phillips NA, Chertkow H, Leblanc MM, Pim H, Murtha S. Functional and anatomical memory indices in patients with or at risk for Alzheimer's disease. J Int Neuropsychol Soc. 2004 Mar;10(2):200-10. | CrossRef | PubMed |
  38. Polich J, Pollock VE, Bloom FE. Meta-analysis of P300 amplitude from males at risk for alcoholism. Psychol Bull. 1994 Jan;115(1):55-73. | CrossRef | Link |
  39. Rao KM, Ananthnarayanan CV, Gangadhar BN, Janakiramaiah N. Smaller auditory P300 amplitude in schizophrenics in remission. Neuropsychobiology. 1995;32(3):171-4. | PubMed |
  40. Guerra S, Iglesias J, Matín M, Bravo TM, Mendoza R, Reyes A, et al. Redes neurales de la atención en pacientes con esquizofrenia y sus familiares no afectados de primer grado: un endofenotipo potencial. Actas Esp. Psiquiatr. 2011;39(1):32-44. | Link |
  41. Martín-Reyes M, Mendoza R, Domínguez M, Caballero A, Bravo TM, Díaz T, et al. Depressive symptoms evaluated by the Calgary Depression Scale for Schizophrenia (CDSS): genetic vulnerability and sex effects. Psychiatry Res. 2011 Aug 30;189(1):55-61. | CrossRef | PubMed |
  42. Sponheim SR, McGuire KA, Stanwyck JJ. Neural anomalies during sustained attention in first-degree biological relatives of schizophrenia patients. Biol Psychiatry. 2006 Aug 1;60(3):242-52. | CrossRef | PubMed |
  43. Mendoza R, Cabral-Calderin Y, Domínguez M, Garcia A, Borrego M, Caballero A, et al. Impairment of emotional expression recognition in schizophrenia: a Cuban familial association study. Psychiatry Res. 2011 Jan 30;185(1-2):44-8. | CrossRef | PubMed |
Amenedo E, Díaz F. Aging-related changes in processing of non-target and target stimuli during an auditory oddball task. Biol Psychol. 1998 Aug;48(3):235-67. | PubMed |

American Psychiatric Association. DSM-IV. Diagnostic and statistical manual of mental disorders, 4 ed, Washington, DC: American Psychiatric Association, 1994.

Braff DL. Psychophysiological and information processing approaches to schizophrenia. En: Neurobiological foundation of mental illness. New York: Oxford University Press, 1999:258-271.

Blackwood DH, Young AH, McQueen JK, Martin MJ, Roxborough HM, Muir WJ, et al. Magnetic resonance imaging in schizophrenia: altered brain morphology associated with P300 abnormalities and eye tracking dysfunction. Biol Psychiatry. 1991 Oct;30(8):753-69. | PubMed |

Bharath S, Gangadhar BN, Janakiramaiah N. P300 in family studies of schizophrenia: review and critique. Int J Psychophysiol. 2000 Oct;38(1):43-54. | PubMed |

Boutros N, Nasrallah H, Leighty R, Torello M, Tueting P, Olson S. Auditory evoked potentials in schizophrenia. Biol Psychiatry. 1996;39(7):651. | CrossRef |

Bramon E, McDonald C, Croft RJ, Landau S, Filbey F, Gruzelier JH, et al. Is the P300 wave an endophenotype for schizophrenia? A meta-analysis and a family study. Neuroimage. 2005 Oct 1;27(4):960-8. | PubMed |

Brown KJ, Gonsalvez CJ, Harris AW, Williams LM, Gordon E. Target and non-target ERP disturbances in first episode vs. chronic schizophrenia. Clin Neurophysiol. 2002 Nov;113(11):1754-63. | CrossRef | PubMed |

Cohen RA, Sparling-Cohen YA, O’Donnell BF. The Neuropsychology of Attention. New York: Plenum Press, 1993.

Donchin E, Coles MGH. Is the P300 component a manifestation of context updating ? Behav Brain Sci. 1988;11(3):357-373. | CrossRef |

Debruille JB, Schneider-Schmid A, Dann P, King S, Laporta M, Bicu M. The correlation between positive symptoms and left temporal event-related potentials in the P300 time window is auditory specific and training sensitive. Schizophr Res. 2005 Oct 15;78(2-3):117-25. | CrossRef | PubMed |

Egan MF, Duncan CC, Suddath RL, Kirch DG, Mirsky AF, Wyatt RJ. Event-related potential abnormalities correlate with structural brain alterations and clinical features in patients with chronic schizophrenia. Schizophrenia Research. 1994;11(3):259-271. | CrossRef |

Fabiani M, Gratton G, Karis D, Donchin E: Definition, identification, and reliability of measurement of the P300 component of the event-related brain potential. En: Advances in Psychophysiology, vol 2. Greenwich, CT: JAI Press, 1987.

Ford JM, Mathalon DH, White PM, Pfefferbaum A. Left temporal deficit of P300 in patients with schizophrenia: effects of task. Int J Psychophysiol. 2000 Oct;38(1):71-9. | PubMed |

Forte A, Bernardo A, Caputo F, Bucci P, Mucci A, Galderisi S, et al. P300 Brain Microstate in deficit and nondeficit schizophrenia. Eur Psychiatr. 2002;17(1):188. | PubMed |

Frodl T, Meisenzahl EM, Müller D, Greiner J, Juckel G, Leinsinger G, et al. Corpus callosum and P300 in schizophrenia. Schizophr Res. 2001 Apr 15;49(1-2):107-19. | CrossRef | PubMed |

Gottesman II, Gould TD. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry. 2003 Apr;160(4):636-45. | CrossRef | PubMed |

Gonul AS, Suer C, Coburn K, Ozesmi C, Oguz A, Yilmaz A. Effects of olanzapine on auditory P300 in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2003 Feb;27(1):173-7. | PubMed |

Grillon C, Courchesne E, Ameli R, Geyer MA, Braff DL. Increased distractibility in schizophrenic patients. Electrophysiologic and behavioral evidence. Arch Gen Psychiatry. 1990 Feb;47(2):171-9. | CrossRef | PubMed |

Guerra S, Ibáñez A, Martín M, Bobes MA, Reyes A, Mendoza R, et al. N400 deficits from semantic matching of pictures in probands and first-degree relatives from multiplex schizophrenia families. Brain Cogn. 2009 Jul;70(2):221-30. | CrossRef | PubMed |

Higashima M, Kawasaki Y, Urata K, Sakai N, Nagasawa T, Koshino Y, et al. Regional cerebral blood flow in male schizophrenic patients performing an auditory discrimination task. Schizophr Res. 2000 Mar 16;42(1):29-39. | CrossRef | PubMed |

Shaikh M, Hall MH, Schulze K, Dutt A, Li K, Williams I, Walshe M, et al. Effect of DISC1 on the P300 waveform in psychosis. Schizophr Bull. 2013 Jan;39(1):161-7. | CrossRef | PubMed |

Havermans R, Honig A, Vuurman EF, Krabbendam L, Wilmink J, Lamers T, et al. A controlled study of temporal lobe structure volumes and P300 responses in schizophrenic patients with persistent auditory hallucinations. Schizophr Res. 1999 Aug 17;38(2-3):151-8. | PubMed |

Hotchkiss AP, Harvey PD. Effect of concurrent distraction on thought disorder in schizophrenia. American Journal of Psychiatry. 1990;147(2):153-156.

Díaz-Anzaldúa A, Velázquez-Pérez J, Berlanga C. Endophenotypes and biomarkers: an approach to molecular genetic studies of mental disorders. Salud Mental 2013;36(3):161-168. | Link |

Ogura C, Nageishi Y, Omura F, Fukao K, Ohta H, Kishimoto A, er al. N200 component of event-related potentials in depression. Biol Psychiatry. 1993 May 15;33(10):720-6. | CrossRef | PubMed |

Meisenzahl EM, Frodl T, Müller D, Schmitt G, Gallinat J, Zetzsche T, et al. Superior temporal gyrus and P300 in schizophrenia: a combined ERP/structural magnetic resonance imaging investigation. J Psychiatr Res. 2004 Mar-Apr;38(2):153-62. | CrossRef | PubMed |

McCarley RW, O’Donnell BF, Niznikiewicz MA, Salisbury DF, Potts GF, Hirayasu Y, et al. Update on electrophysiology in schizophrenia. Int Rev Psychiatry. 1997;9(4):373-386. | CrossRef |

Matthysse S, Holzman PS, Lange K. The genetic transmission of schizophrenia: application of Mendelian latent structure analysis to eye tracking dysfunctions in schizophrenia and affective disorder. J Psychiatr Res. 1986;20(1):57-67. | PubMed |

Moser RK, Cienfuegos A, Barros J, Javitt D. Auditory distraction and thought disorder in chronic schizophrenic inpatients. Evidence for separate contributions by incapacity and poor allocation and a subsyndrome related to the allocation deficit. Schizophr Res. 2001 Sep 1;51(2-3):163-70. | CrossRef | PubMed |

Vázquez- Barquero JL, et al. Report on the Spanish Translation of the SCAN, Schedules and Glossary. Informe a la Organización Mundial de la Salud. Santander, España: Unidad de Investigación en Psiquiatría Social de Cantabria, 1992.

Kay SR, Fiszbein A, Vital-Herne M, Fuentes LS. The Positive and Negative Syndrome Scale--Spanish adaptation. J Nerv Ment Dis. 1990 Aug;178(8):510-7. | PubMed |

Bunney WE Jr, Hetrick WP, Bunney BG, Patterson JV, Jin Y, Potkin SG, Sandman CA. Structured Interview for Assessing Perceptual Anomalies (SIAPA). Schizophr Bull. 1999;25(3):577-92. | CrossRef | PubMed |

Frangou S, Sharma T, Alarcon G, Sigmudsson T, Takei N, Binnie C, Murray RM. The Maudsley Family Study, II: Endogenous event-related potentials in familial schizophrenia. Schizophr Res. 1997 Jan 17;23(1):45-53. | CrossRef | PubMed |

Schreiber H, Stolz-Born G, Rothmeier J, Kornhuber A, Kornhuber HH, Born J. Endogenous event-related brain potentials and psychometric performance in children at risk for schizophrenia. Biol Psychiatry. 1991 Jul 15;30(2):177-89. | CrossRef | PubMed |

Surwillo WW. Cortical evoked potentials in monozygotic twins and unrelated subjects: comparisons of exogenous and endogenous components. Behav Genet. 1980 Mar;10(2):201-9. | PubMed |

Phillips NA, Chertkow H, Leblanc MM, Pim H, Murtha S. Functional and anatomical memory indices in patients with or at risk for Alzheimer's disease. J Int Neuropsychol Soc. 2004 Mar;10(2):200-10. | CrossRef | PubMed |

Polich J, Pollock VE, Bloom FE. Meta-analysis of P300 amplitude from males at risk for alcoholism. Psychol Bull. 1994 Jan;115(1):55-73. | CrossRef | Link |

Rao KM, Ananthnarayanan CV, Gangadhar BN, Janakiramaiah N. Smaller auditory P300 amplitude in schizophrenics in remission. Neuropsychobiology. 1995;32(3):171-4. | PubMed |

Guerra S, Iglesias J, Matín M, Bravo TM, Mendoza R, Reyes A, et al. Redes neurales de la atención en pacientes con esquizofrenia y sus familiares no afectados de primer grado: un endofenotipo potencial. Actas Esp. Psiquiatr. 2011;39(1):32-44. | Link |

Martín-Reyes M, Mendoza R, Domínguez M, Caballero A, Bravo TM, Díaz T, et al. Depressive symptoms evaluated by the Calgary Depression Scale for Schizophrenia (CDSS): genetic vulnerability and sex effects. Psychiatry Res. 2011 Aug 30;189(1):55-61. | CrossRef | PubMed |

Sponheim SR, McGuire KA, Stanwyck JJ. Neural anomalies during sustained attention in first-degree biological relatives of schizophrenia patients. Biol Psychiatry. 2006 Aug 1;60(3):242-52. | CrossRef | PubMed |

Mendoza R, Cabral-Calderin Y, Domínguez M, Garcia A, Borrego M, Caballero A, et al. Impairment of emotional expression recognition in schizophrenia: a Cuban familial association study. Psychiatry Res. 2011 Jan 30;185(1-2):44-8. | CrossRef | PubMed |