Top

Journal of Autism and Developmental Disorders

Gepubliceerd in:

01-02-2015 | Original Paper

Eyeblink Conditioning: A Non-invasive Biomarker for Neurodevelopmental Disorders

Auteurs: Bethany C. Reeb-Sutherland, Nathan A. Fox

Gepubliceerd in: Journal of Autism and Developmental Disorders | Uitgave 2/2015

Abstract

Eyeblink conditioning (EBC) is a classical conditioning paradigm typically used to study the underlying neural processes of learning and memory. EBC has a well-defined neural circuitry, is non-invasive, and can be employed in human infants shortly after birth making it an ideal tool to use in both developing and special populations. In addition, abnormalities in the cerebellum, a region of the brain highly involved in EBC, have been implicated in a number of neurodevelopmental disorders including autism spectrum disorders (ASDs). In the current paper, we review studies that have employed EBC as a biomarker for several neurodevelopmental disorders including fetal alcohol syndrome, Down syndrome, fragile X syndrome, attention deficit/hyperactivity disorder, dyslexia, specific language impairment, and schizophrenia. In addition, we discuss the benefits of using such a tool in individuals with ASD.

vorige artikel An Electrophysiological Investigation of Interhemispheric Transfer Time in Children and Adolescents with High-Functioning Autism Spectrum Disorders

volgende artikel Neuromagnetic Oscillations Predict Evoked-Response Latency Delays and Core Language Deficits in Autism Spectrum Disorders

Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 13, 232–240.PubMed

Allin, M., et al. (2001). Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain, 124, 60–66.PubMed

Amaral, D. G., Schumann, C. M., & Nordahl, C. W. (2008). Neuroanatomy of autism. Trends in Neurosciences, 31, 137–145.PubMed

Andreasen, N. C., Paradiso, S., & O’Leary, D. S. (1998). “Cognitive dysmetria” as an integrative theory of schizophrenia: A dysfunction in cortical-subcortical-cerebellar circuitry? Schizophrenia Bulletin, 24, 203–218.PubMed

Andreasen, N. C., & Pierson, R. (2008). The role of the cerebellum in schizophrenia. Biological Psychiatry, 64, 81–88.PubMedCentralPubMed

Andreasen, N. C., et al. (1996). Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. Proceedings of the National Academy of Sciences of the United States of America, 93, 9985–9990.PubMedCentralPubMed

APA. (2000). Diagnostic and statistical manual of mental disorders IV-TR. Washington, DC: American Psychiatric Association.

Aylward, G. (2002). Cognitive and neuropsychological outcomes: More than IQ scores. Mental Retardation and Developmental Disabilities Research Reviews, 8, 234–240.PubMed

Berquin, P. C., et al. (1998). Cerebellum in attention-deficit hyperactivity disorder: A morphometric MRI study. Neurology, 50, 1087–1093.PubMed

Berthier, N. E., & Moore, J. W. (1990). Activity of deep cerebellar nuclear cells during classical conditioning of nictitating membrane extension in rabbits. Experimental Brain Research, 63, 44–54.

Bolbecker, A. R., Mehta, C. S., Edwards, C. R., Steinmetz, J. E., O’Donnell, B. F., & Hetrick, W. P. (2009). Eye-blink conditioning deficits indicate temporal processing abnormalities in schizophrenia. Schizophrenia Research, 111, 182–191.PubMedCentralPubMed

Bolbecker, A. R., et al. (2011). Exploration of cerebellar-dependent associative learning in schizophrenia: effects of varying and shifting interstimulus interval on eyeblink conditioning. Behavioral Neuroscience, 125, 687–698.PubMedCentralPubMed

Bolduc, M. E., et al. (2011). Spectrum of neurodevelopmental disabilities in children with cerebellar malformations. Developmental Medicine and Child Neurology, 53, 409–416.PubMed

Brown, S. M., et al. (2005). Eyeblink conditioning deficits indicate timing and cerebellar abnormalities in schizophrenia. Brain and Cognition, 58, 94–108.PubMed

Brunet, E., Sarfati, Y., Hardy-Bayle, M. C., & Decety, J. (2000). A PET investigation of the attribution of intentions with a nonverbal task. NeuroImage, 11, 157–166.PubMed

Calarge, C., Andreasen, N. C., & O’Leary, D. S. (2003). Visualizing how one brain understands another: A PET study of theory of mind. American Journal of Psychiatry, 160, 1954–1964.PubMed

Castellanos, F. X., et al. (2002). Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. Journal of the American Medical Association, 288, 1740–1748.PubMed

Catts, H. W. (2004). Language impairments and reading disabilities. In R. D. Kent (Ed.), The MIT Encyclopedia of communication disorders (pp. 329–331). Cambridge, MA: MIT.

Chapman, R. S., & Hesketh, L. J. (2000). Behavioral phenotype of individuals with Down syndrome. Mental Retardation and Developmental Disabilities Research Reviews, 6, 84–95.PubMed

Cheng, D. T., Disterhoft, J. F., Power, J. M., Ellis, D. A., & Desmond, J. E. (2008). Neural substrates underlying human delay and trace eyeblink conditioning. Proceedings of the National Academy of Sciences of the United States of America, 105, 8108–8113.PubMedCentralPubMed

Christian, K. M., & Thompson, R. F. (2003). Neural substrates of eyeblink conditioning: acquisition and retention. Learning & Memory, 11, 427–455.

Claflin, D. I., Stanton, M. E., Herbert, J. S., Greer, J., & Eckerman, C. O. (2002). Effect of delay interval on classical eyeblink conditioning in 5-month-old human infants. Developmental Psychobiology, 41, 329–340.PubMed

Coffin, J. M., Baroody, S., Schneider, K., & O’Neill, J. (2005). Impaired cerebellar learning in children with prenatal alcohol exposure: A comparative study of eyeblink conditioning in children with ADHD and dyslexia. Cortex, 41, 389–398.PubMed

Courchesne, E. (1997). Brainstem, cerebellar and limbic neuroanatomical abnormalities in autism. Current Opinion in Neurobiology, 7, 269–278.PubMed

Courchesne, E., Redcay, E., Morgan, J. T., & Kennedy, D. P. (2005). Autism at the beginning: Microstructural and growth abnormalities underlying the cognitive and behavioral phenotype of autism. Development and Psychopathology, 17, 577–597.PubMed

Courchesne, E., et al. (2007). Mapping early brain development in autism. Neuron, 56, 1–15.

Cromwell, R., Palk, B., & Folshee, J. (1961). Studies in activity level: The relationships among eyelid conditioning, intelligence, activity level, and age. American Journal of Mental Deficiency, 65, 744–748.PubMed

D’Agata, F., et al. (2011). The recognition of facial emotions in spinocerebellar ataxia patients. Cerebellum, 10, 600–610.PubMed

Dawson, G., et al. (2010). Randomized, controlled trial of an intervention for toddlers with autism: The Early Start Denver Model. Pediatrics, 125, e17–e23.PubMed

Dawson, G., et al. (2012). Early behavioral intervention is associated with normalized brain activity in young children with autism. Journal of the American Academy of Child and Adolescent Psychiatry, 51, 1150–1159.PubMedCentralPubMed

de Kieviet, J. F., Zoetebier, L., van Elburg, R. M., Vermeulen, R. J., & Oosterlaan, J. (2012). Brain development of very preterm and very low-birthweight children in childhood and adolescence: A meta-analysis. Developmental Medicine and Child Neurology, 54, 313–323.PubMed

De Vries, B. B., et al. (1997). Screening and diagnosis for the fragile X syndrome among the mentally retarded: an epidemiological and psychological survey. Collaborative Fragile X Study Group. American Journal of Human Genetics, 61, 660–667.PubMedCentralPubMed

DeCasper, A. J., & Fifer, W. P. (1980). Of human bonding: Newborns prefer their mothers’ voices. Science, 208, 1174–1176.PubMed

Edwards, C. R., et al. (2008). Cerebellum volume and eyeblink conditioning in schizophrenia. Psychiatry Research: Neuroimaging, 162, 185–194.PubMedCentralPubMed

Eigsti, I. M., & Shapiro, T. (2003). A systems neuroscience approach to autism: Biological, cognitive, and clinical perspectives. Mental Retardation and Developmental Disabilities, 9, 205–215.

Fifer, W. P., et al. (2010). Newborn infants learn during sleep. Proceedings of the National Academy of Sciences of the United States of America, 107, 10320–10323.PubMedCentralPubMed

Fitzgerald, H. E., & Brackbill, Y. (1976). Classical conditioning in infancy: Development and constraints. Psychological Bulletin, 83, 353–376.PubMed

Foroud, T., et al. (2012). Relation over time between facial measurements and cognitive outcomes in fetal alcohol-exposed children. Alcoholism: Clinical and Experimental Research, 36, 1634–1646.

Forsyth, J. K., et al. (2012). Cerebellar-dependent eyeblink conditioning deficits in schizophrenia spectrum disorders. Schizophrenia Bulletin, 38, 751–759.PubMedCentralPubMed

Frings, M., et al. (2010). Timing of conditioned eyeblink responses is impaired in children with attention-deficit/hyperactivity disorder. Experimental Brain Research, 201, 167–176.PubMed

Garcia, K. S., & Mauk, M. D. (1998). Pharmacological analysis of cerebellar contributions to the timing and expression of conditioned eyelid responses. Neuropharmacology, 37, 471–480.PubMed

Garcia, K. S., Steele, P. M., & Mauk, M. D. (1999). Cerebellar cortex lesions prevent acquisition of conditioned eyelid responses. Journal of Neuroscience, 19, 1940–10947.

Gergely, G., & Watson, J. S. (1996). The social biofeedback theory of parental affect-mirroring: The development of emotional self-awareness and self-control in infancy. International Journal of Psychoanalysis, 77, 1181–1212.PubMed

Gerwig, M., Kolb, F. P., & Timmann, D. (2007). The involvement of the human cerebellum in eyeblink conditioning. Cerebellum, 6, 38–57.PubMed

Gleichgerrcht, E., Torralva, T., Rattazzi, A., Marenco, V., Roca, M., & Manes, F. (2012). Selective impairment of cognitive empathy for moral judgment in adults with high functioning autism. Social Cognitive and Affective Neuroscience, in press.

Gothelf, D., et al. (2008). Neuroanatomy of fragile X syndrome is associated with aberrant behavior and the fragile X mental retardation protein (FMRP). Annals of Neurology, 63, 40–51. doi:10.1002/ana.21243.PubMedCentralPubMed

Green, J. T. (2004). The effects of ethanol on the developing cerebellum and eyeblink conditioning. Cerebellum, 3, 178–187.

Green, J. T., Rogers, R. F., Goodlett, C. R., & Steinmetz, J. E. (2000). Impairment in eyeblink conditioning in adult rats exposed to ethanol as neonates. Alcoholism, Clinical and Experimental Research, 24, 438–447.PubMed

Hagerman, R. J., & Hagerman, P. J. (2002). The fragile X premutation: Into the phenotypic fold. Current Opinion in Genetics & Development, 12, 278–283.

Hammock, E. A., & Levitt, P. (2006). The discipline of neurobehavioral development: The emerging interface that builds processes and skills. Human Development, 49, 294–309.

Hardiman, M. J., Ramnani, N., & Yeo, C. H. (1996). Reversible inactivations of the cerebellum with muscimol prevent the acquisition and extinction of conditioned nictitating membrane responses in the rabbit. Experimental Brain Research, 110, 235–247.PubMed

Hart, A. R., Whitby, E. W., Griffiths, P. D., & Smith, M. F. (2008). Magnetic resonance imaging and developmental outcome following preterm birth: Review of current evidence. Developmental Medicine and Child Neurology, 50, 655–663.PubMed

Herbert, J. S., Eckerman, C. O., Goldstein, R. F., & Stanton, M. E. (2004). Contrasts in infant classical eyeblink conditioning as a function of premature birth. Infancy, 5, 367–383.

Herbert, J. S., Eckerman, C. O., & Stanton, M. E. (2003). The ontogeny of human learning in delay, long-delay, and trace eyeblink conditioning. Behavioral Neuroscience, 117, 1196–1210.PubMed

Hessl, D., Rivera, S. M., & Reiss, A. L. (2004). The neuroanatomy and neuroendocrinology of fragile x syndrome. Mental Retardation and Developmental Disabilities Research Review, 10, 17–24.

Hill, E. L. (2001). Non-specific nature of specific language impairment: A review of the literature with regard to concomitant motor impairments. International Journal of Language and Communication Disorders, 36, 149–171.PubMed

Hinds, H. L., et al. (1993). Tissue specific expression of FMR-1 provides evidence for a functional role in fragile x syndrome. Nature Genetics, 3, 36–43. doi:10.1038/ng0193-36.PubMed

Hofer, E., Doby, D., Anderer, P., & Dantendorfer, K. (2001). Impaired conditional discrimination learning in schizophrenia. Schizophrenia Research, 51, 127–136.PubMed

Hoffman, H. S., Cohen, M. E., & DeVido, C. J. (1985). A comparison of classical eyelid conditioning in adults and infants. Infant Behavior and Development, 8, 247–254.

Hoyme, H. E., et al. (2005). A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: Clarification of the 1996 Institute of Medicine criteria. Pediatrics, 115, 39–47.PubMed

Insel, T. R. (2010). Rethinking schizophrenia. Nature, 468, 187–193.PubMed

Ivkovich, D., Collins, K. L., Eckerman, C. O., Krasnegor, N. A., & Stanton, M. E. (1999). Classical delay eyeblink conditioning in 4- and 5-month-old human infants. Psychological Science, 10, 4–8.

Ivkovich, D., Eckman, C. O., Krasnegor, N. A., & Stanton, M. E. (2000). Using eyeblink conditioning to assess neurocognitive development in human infants. In D. S. Woodruff-Pak, & J. E. Steinmetz (Eds.), Eyeblink classical conditioning: Volume 1 applications in humans (pp. 119–142). Norwell, MA: Kluwer Academic Publishers.

Jacobson, S. W., et al. (2008). Impaired eyeblink conditioning in children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 32, 365–372.PubMed

Jacobson, S. W., et al. (2011). Impaired delay and trace eyeblink conditioning in school-age children with fetal alcohol syndrome. Alcoholism, Clinical and Experimental Research, 35, 1–15.

Kaufmann, W. E., et al. (2004). Autism spectrum disorder in fragile X syndrome: Communication, social interaction, and specific behaviors. American Journal of Medical Genetics Part A, 129A, 225–234.PubMed

Kim, J. J., Clark, R. E., & Thompson, R. F. (1995). Hippocampectomy impairs the memory of recent, but not remotely, acquired trace eyeblink conditioned responses. Behavioral Neuroscience, 109, 195–203.PubMed

Klin, A., Lin, D. J., Gorrindo, P., Ramsay, G., & Jones, W. (2009). Two-year-olds with autism orient to non-social contingencies rather than biological motion. Nature, 459, 257–263.PubMedCentralPubMed

Koekkoek, S. K. E., et al. (2005). Deletion of FMR1 in Purkinje cells enhances parallel fiber LTD, enlarges spines, and attenuates cerebellar eyelid conditioning in Fragile X syndrome. Neuron, 47, 339–352.PubMed

Krain, A. L., & Castellanos, F. X. (2006). Brain development and ADHD. Clinical Psychology Review, 26, 433–444.PubMed

Laasonen, M., et al. (2012). Project DyAdd: Classical eyeblink conditioning in adults with dyslexia and ADHD. Experimental Brain Research, 223, 19–32.PubMed

Lai, F., & Williams, R. S. (1989). A prospective study of Alzheimer disease in Down syndrome. Archives of Neurology, 46, 849–853.PubMed

LeJeune, J., Gautier, M., & Turpin, R. (1959). Study of somatic chromosomes from 9 mongoloid children. Comptes Renus de l’Academic les Sciences, 248, 1721–1722.

Lewis, D. A., & Levitt, P. (2002). Schizophrenia as a disorder of neurodevelopment. Annual Review of Neuroscience, 25, 409–432.PubMed

Limperopoulos, C., et al. (2007). Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics, 120, 584–593.PubMed

Linkersdorfer, J., Lonnemann, J., Lindberg, S., Hasselhorn, M., & Fiebach, C. J. (2012). Grey matter alterations co-localize with functional abnormalities in developmental dyslexia: An ALE meta-analysis. PLoS ONE, 7, e43122.PubMedCentralPubMed

Lintz, L. M., Fitzgerald, H. E., & Brackbill, Y. (1967). Conditioning the eyeblink response to sound in infants. Psychonomic Science, 7, 405–406.

Little, A. H., Lipsitt, L. P., & Rovee-Collier, C. (1984). Classical conditioning and retention of the infant’s eyelid response: Effects of age and interstimulus interval. Journal of Experimental Child Psychology, 37, 512–524.PubMed

Marenco, S., Weinberger, D. R., & Schreurs, B. G. (2003). Single-cue delay and trace classical conditioning in schizophrenia. Biological Psychiatry, 53, 390–402.PubMed

McCormick, D. A., Steinmetz, J. E., & Thompson, R. F. (1985). Lesions of the inferior olivary complex cause extinction of the classically conditioned eyeblink response. Brain Research, 271, 73–88.

McCormick, D. A., & Thompson, R. F. (1984). Neuronal responses of the rabbit cerebellum during acquisition and performance of a classically conditioned nictitating membrane-eyelid response. Journal of Neuroscience, 4, 2811–2822.PubMed

Morgan, J. J. B., & Morgan, S. S. (1944). Infant learning as a developmental index. Journal of Genetic Psychology, 65, 281–289.

Moyer, J. F., Deyo, R. A., & Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience, 104, 243–252.PubMed

Naito, T., & Lipsitt, L. P. (1969). Two attempts to condition eyelid responses in human infants. Journal of Experimental Child Psychology, 8, 263–270.PubMed

Nicolson, R. I., Daum, I., Schugens, M. M., Fawcett, A. J., & Schulz, A. (2002). Eyeblink conditioning indicates cerebellar abnormality in dyslexia. Experimental Brain Research, 143, 42–50.PubMed

Nicolson, R. I., Fawcett, A. J., Berry, E. L., Jenkins, I. H., Dean, P., & Brooks, D. J. (1999). Association of abnormal cerebellar activation with motor learning difficulties in dyslexic adults. Lancet, 353, 1662–1667.PubMed

Nicolson, R. I., Fawcett, A. J., & Dean, P. (2001). Developmental dyslexia: The cerebellar deficit hypothesis. Trends in Neurosciences, 24, 508–511.PubMed

O’Connor, N., & Rawnsley, K. (1959). Two types of conditioning in psychotics and normals. Journal of Abnormal and Social Psychology, 58, 157–161.

O’Halloran, C. J., Kinsella, G. J., & Storey, E. (2012). The cerebellum and neuropsychological functioning: A critical review. Journal of Clinical and Experimental Neuropsychology, 34, 35–56.PubMed

Ohlrich, E. S., & Ross, L. E. (1968). Acquisition and differential conditioning of the eyelid response in normal and retarded children. Journal of Experimental Child Psychology, 6, 181–193.PubMed

Pennington, B. F., Moon, J., Edgin, J., Stedron, J., & Nadel, L. (2003). The neuropsychology of Down syndrome: Evidence for hippocampal dysfunction. Child Development, 74, 75–93.PubMed

Perrett, S. P., & Mauk, M. D. (1995). Extinction of conditioned eyelid responses requires the anterior lobe of the cerebellar cortex. Journal of Neuroscience, 15, 2074–2080.PubMed

Perrett, S. P., Ruiz, B. P., & Mauk, M. D. (1993). Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. Journal of Neuroscience, 13, 1708–1718.PubMed

Ramnani, N., & Yeo, C. H. (1996). Reversible inactivations of the cerebellum prevent the extinction of conditioned nictitating membrane responses in rabbits. Journal of Physiology, 495, 159–168.PubMedCentralPubMed

Rapoport, J. (2001). The cerebellum in psychiatric disorders. International Review of Psychiatry, 13, 295–301.

Reeb-Sutherland, B. C., Fifer, W. P., Byrd, D. L., Hammock, E. A. D., Levitt, P., & Fox, N. A. (2011). One-month-old human infants learn about the social world while they sleep. Developmental Science, 14, 1134–1141.PubMedCentralPubMed

Reeb-Sutherland, B. C., Levitt, P., & Fox, N. A. (2012). The predictive nature of individual differences in early associative learning and emerging social behavior. PLoS ONE, 7, e30511.PubMedCentralPubMed

Rendle-Short, J. (1961). The puff test: An attempt to assess the intelligence of young children by use of a conditioned reflex. Archives of Diseases of Childhood, 36, 50–57.

Rochat, P., & Striano, T. (1999). Social-cognitive development in the first year. In P. Rochat (Ed.), Early social cognition: Understanding others in the first months of life (pp. 3–34). Mahwah: Lawrence Erlbaum Associates.

Rogers, S. J. (2009). What are infant siblings teaching us about autism in infancy? Autism Research, 2, 125–137.PubMedCentralPubMed

Ross, L. E., Headrick, M. W., & MacKay, P. B. (1967). Classical eyelid conditioning in young mongoloid children. Journal of Mental Deficiency, 72, 21–29.

Ross, L. E., Koski, C. H., & Yeager, J. (1964). Classical eyelid conditioning of the severely retarded: Partial reinforcement effects. Psychonomic Science, 1, 253–254.

Rovee-Collier, C., & Lipsitt, L. P. (1982). Learning, adaptation, and memory in the newborn. In P. Stratton (Ed.), Psychobiology of the human newborn (pp. 147–190). Chichester: Wiley.

Schmahmann, J. D., Weilburg, J. B., & Sherman, J. C. (2007). The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum, 6, 254–267.PubMed

Schmajuk, N. A., & DiCarlo, J. J. (1991). A neural network approach to hippocampal function in classical conditioning. Behavioral Neuroscience, 105, 82–110.PubMed

Sears, L. L., Andreasen, N. C., & O’Leary, D. S. (2000). Cerebellar functional abnormalities in schizophrenia are suggested by classical eyeblink conditioning. Biological Psychiatry, 48, 204–209.PubMed

Sears, L. L., Finn, P. R., & Steinmetz, J. E. (1994). Abnormal classical eye-blink conditioning in autism. Journal of Autism and Developmental Disorders, 24, 737–751.PubMed

Sears, L. L., & Steinmetz, J. E. (1990). Haloperidol impairs classically conditioned nictitating membrane responses and conditioning-related cerebellar interpositus nucleus activity in rabbits. Pharmacology, Biochemistry and Behavior, 36, 821–830.PubMed

Senju, A., Southgate, V., White, S., & Frith, U. (2009). Mindblind eyes: An absence of spontaneous theory of mind in Asperger syndrome. Science, 325, 883–885.PubMed

Shamay-Tsoory, S. G., et al. (2005). The neural correlates of understanding the other’s distress: A positron emission tomography investigation of accurate empathy. NeuroImage, 27, 468–472.PubMed

Shaywitz, S., & Shaywitz, B. (2003). Dyslexia: specific reading disability. Pediatric Review, 24, 147–153.

Smit, A. E., et al. (2008). Savings and extinction of conditioned eyeblink responses in fragile X syndrome. Genes, Brain and Behavior, 7, 770–777.

Sokolov, A. A., Erb, M., Gharabaghi, A., Grodd, W., Tatagiba, M. S., & Pavlova, M. (2012). Biological motion processing: The left cerebellum communicates with the right superior temporal sulcus. NeuroImage, 59, 2824–2830.PubMed

Sokolov, A. A., Gharabaghi, A., Tatagiba, M. S., & Pavlova, M. (2010). Cerebellar engagement in an action observation network. Cerebral Cortex, 20, 486–491.PubMed

Solomon, P. R., Vander Shaaf, E. R., Thompson, R. F., & Weisz, D. J. (1986). Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behavioral Neuroscience, 100, 729–744.PubMed

Spain, B. (1966). Eyelid conditioning and arousal in schizophrenic and normal subjects. Journal of Abnormal Psychology, 71, 260–266.PubMed

Spottiswoode, B. S., et al. (2011). Diffusion tensor imaging of the cerebellum and eyeblink conditioning in fetal alcohol spectrum disorder. Alcoholism, Clinical and Experimental Research, 35, 2174–2183.PubMedCentralPubMed

Stanfield, A. C., McIntosh, A. M., Spencer, M. D., Philip, R., Gaur, S., & Lawrie, S. M. (2008). Towards a neuroanatomy of autism: A systematic review and meta-analysis of structural magnetic resonance imaging studies. European Psychiatry, 23, 289–299.PubMed

Stanton, M. E., Claflin, D. I., & Herbert, J. S. (2010). Ontogeny of multiple memory systems: Eyeblink conditioning in rodents and humans. In M. S. Blumberg, J. H. Freeman, & Robinson, S. R. (Eds.), Oxford handbook of developmental behavioral neuroscience (pp. 501–526). New York: Oxford University Publishing.

Stanton, M. E., & Goodlett, C. R. (1998). Neonatal ethanol exposure impairs eyeblink conditioning. Alcoholism, Clinical and Experimental Research, 22, 270–275.PubMed

Steinmetz, J. E., & Rice, M. L. (2010). Cerebellar-dependent delay eyeblink conditioning in adoloscents with Specific Language Impairment. Journal of Neurodevelopmental Disorders, 2, 243–251.PubMedCentralPubMed

Stern, D. N. (2000). The interpersonal world of the infant. New York: Basic Books.

Tarabulsy, G. M., Tessier, R., & Kappas, A. (1996). Contingency detection and the contingent organization of behavior in interactions: Implications for socioemotional development in infancy. Psychological Bulletin, 120, 25–41.PubMed

Taylor, J. A., & Spence, K. W. (1954). Conditioning level in the behavior disorders. Journal of Abnormal and Social Psychology, 49, 497–503.

Tobia, M. J., & Woodruff-Pak, D. S. (2009). Delay eyeblink classical conditioning is impaired in fragile X syndrome. Behavioral Neuroscience, 123, 665–676.PubMedCentralPubMed

Trevarthen, C. (1979). The foundations of intersubjectivity: development of interpersonal and cooperative understanding in infants. In D. Olson (Ed.), The social foundations of language and thought (pp. 316–342). New York: W.W. Norton & Co.

Verkerk, A., et al. (1991). Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell, 65, 905–914. doi:10.1016/0092-8674(91)90397-h.PubMed

Watson, J. S. (1966). The development of generalization of “contingency awareness” in early infancy: some hypotheses. Merril Palmer Quarterly, 12, 123–155.

Wenger, M. A. (1936). An investigation of conditioned responses in human infants. University of Iowa Studies in Child Welfare, 12, 9–90.

Werden, D., & Ross, L. E. (1972). A comparison of the trace and delay classical conditioning performance of normal children. Journal of Experimental Child Psychology, 14, 126–132.PubMed

Wisniewski, K. E., Wisniewski, H. M., & Wen, G. Y. (1985). Occurence of neuropathological changes and dementia of Alzheimer’s disease in Down’s syndrome. Annals of Neurology, 17, 278–282.PubMed

Woodruff-Pak, D. S., & Disterhoft, J. F. (2008). Where is the trace in trace conditioning? Trends in Neurosciences, 31, 105–112.PubMed

Woodruff-Pak, D. S., Papka, M., & Simon, E. W. (1994). Eyeblink classical conditioning in Down’s syndrome, Fragile X syndrome, and normal adults over and under age 35. Neuropsychology, 8, 14–24.

Woodruff-Pak, D. S., Romano, S., & Papka, M. (1996). Training to criterion in eyeblink classical conditioning in Alzheimer’s disease, Down’s syndrome with Alzheimer’s disease, and healthy elderly. Behavioral Neuroscience, 110, 22–29.PubMed

Woodruff-Pak, D. S., & Steinmetz, J. E. (Eds.). (2000a). Eyeblink classical conditioning: Volume 1 applications in humans. Norwell, MA: Kluwer Academic Publishers.

Woodruff-Pak, D. S., & Steinmetz, J. E. (Eds.). (2000b). Eyeblink classical conditioning: Volume 2 animal models. Norwell, MA: Kluwer Academic Publishers.

Yung, A. R., McGorry, P. D., McFarlane, C. A., Jackson, H. J., Patton, G. C., & Rakkar, A. (1996). Monitoring and care of young people at incipient risk of psychosis. Schizophrenia Bulletin, 22, 283–303.PubMed

Yung, A. R., et al. (2003). Psychosis prediction: 12-month follow up of a high-risk (“prodromal”) group. Schizophrenia Research, 60, 21–32.PubMed

Titel: Eyeblink Conditioning: A Non-invasive Biomarker for Neurodevelopmental Disorders
Auteurs: Bethany C. Reeb-Sutherland
Nathan A. Fox
Publicatiedatum: 01-02-2015
Uitgeverij: Springer US
Gepubliceerd in: Journal of Autism and Developmental Disorders / Uitgave 2/2015
Print ISSN: 0162-3257
Elektronisch ISSN: 1573-3432
DOI: https://doi.org/10.1007/s10803-013-1905-9

Andere artikelen Uitgave 2/2015

Autonomic Dysregulation During Sensory Stimulation in Children with Autism Spectrum Disorder

Original Paper

Joint Analysis of Band-Specific Functional Connectivity and Signal Complexity in Autism

Original Paper

Infant Neural Sensitivity to Dynamic Eye Gaze Relates to Quality of Parent–Infant Interaction at 7-Months in Infants at Risk for Autism

Open Access
Original Paper

Attenuated Auditory Event-Related Potentials and Associations with Atypical Sensory Response Patterns in Children with Autism

Original Paper

Realizing the Translational Promise of Psychophysiological Research in ASD

Editorial

Neuromagnetic Oscillations Predict Evoked-Response Latency Delays and Core Language Deficits in Autism Spectrum Disorders

Original Paper