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Selective Attention and the Three-Process Memory Model for the Interpretation of Verbal Free Recall in Amyotrophic Lateral Sclerosis

Published online by Cambridge University Press:  07 June 2012

Foteini Christidi ,
Ioannis Zalonis ,
Nikolaos Smyrnis  and
Ioannis Evdokimidis
Foteini Christidi*
Affiliation:
Postgraduate Program in Clinical Neuropsychology, Medical School, National and Kapodistrian University, Athens, Greece
Ioannis Zalonis
Affiliation:
Neuropsychological Laboratory, First Department of Neurology, Aiginition Hospital, Medical School, National and Kapodistrian University, Athens, Greece
Nikolaos Smyrnis
Affiliation:
First Department of Psychiatry, Aiginition Hospital, Medical School, National and Kapodistrian University, Athens, Greece
Ioannis Evdokimidis
Affiliation:
First Department of Neurology, Aiginition Hospital, Medical School, National and Kapodistrian University, Athens, Greece
*
Correspondence and reprint requests to: Foteini Christidi, 72-74, Vasilissis Sofias Avenue, Aiginition Hospital, 115 28, Athens, Greece. E-mail: [email protected]
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Abstract

The present study investigates selective attention and verbal free recall in amyotrophic lateral sclerosis (ALS) and examines the contribution of selective attention, encoding, consolidation, and retrieval memory processes to patients’ verbal free recall. We examined 22 non-demented patients with sporadic ALS and 22 demographically related controls using Stroop Neuropsychological Screening Test (SNST; selective attention) and Rey Auditory Verbal Learning Test (RAVLT; immediate & delayed verbal free recall). The item-specific deficit approach (ISDA) was applied to RAVLT to evaluate encoding, consolidation, and retrieval difficulties. ALS patients performed worse than controls on SNST (p < .001) and RAVLT immediate and delayed recall (p < .001) and showed deficient encoding (p = .001) and consolidation (p = .002) but not retrieval (p = .405). Hierarchical regression analysis revealed that SNST and ISDA indices accounted for: (a) 91.1% of the variance in RAVLT immediate recall, with encoding (p = .016), consolidation (p < .001), and retrieval (p = .032) significantly contributing to the overall model and the SNST alone accounting for 41.6%; and (b) 85.2% of the variance in RAVLT delayed recall, with consolidation (p < .001) and retrieval (p = .008) significantly contributing to the overall model and the SNST alone accounting for 39.8%. Thus, selective attention, encoding, and consolidation, and to a lesser extent of retrieval, influenced both immediate and delayed verbal free recall. Concluding, selective attention and the memory processes of encoding, consolidation, and retrieval should be considered while interpreting patients’ impaired free recall. (JINS, 2012, 18, 1–10)

Keywords

Selective attentionEncodingConsolidationRetrievalVerbal free recallSporadic ALS
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 18 , Issue 5 , September 2012 , pp. 809 - 818
Copyright
Copyright © The International Neuropsychological Society 2012

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Footnotes

Note: This article is dedicated to the memory of Professor Dimitrios Vassilopoulos.

References

Abrahams, S., Goldstein, L.H., Al-Chalabi, A., Pickering, A., Morris, R.G., Passingham, R.E., Leigh, P.N. (1997). Relation between cognitive dysfunction and pseudobulbar palsy in amyotrophic lateral sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 62, 464–472.CrossRefGoogle ScholarPubMed
Abrahams, S., Leigh, P.N., Harvey, A., Vythelingum, G.N., Grise, D., Goldstein, L.H. (2000). Verbal fluency and executive dysfunction in amyotrophic lateral sclerosis (ALS). Neuropsychologia, 38, 734–747.CrossRefGoogle ScholarPubMed
Agosta, F., Chio, A., Cosottini, M., De Stefano, N., Falini, A., Mascalchi, M., Filippi, M. (2010). The present and the future of neuroimaging in amyotrophic lateral sclerosis. AJNR American Journal of Neuroradiology, 31, 1769–1777.CrossRefGoogle ScholarPubMed
Banich, M.T., Milham, M.P., Atchley, R., Cohen, N.J., Webb, A., Wszalek, T., Magin, R. (2000). fMRI studies of Stroop tasks reveal unique roles of anterior and posterior brain systems in attentional selection. Journal of Cognitive Neuroscience, 12, 988–1000.CrossRefGoogle ScholarPubMed
Bauer, R.M., Tobias, B., Valenstein, E. (1993). Amnesic disorders. In K.M. Heilman and E. Valenstein (Ed.), Clinical Neuropsychology. NY: Oxford University Press.Google Scholar
Bentin, S., Moscovitch, M., Nirhod, O. (1998). Levels of processing and selective attention effects on encoding in memory. Acta Psychologica, 98, 311–341.CrossRefGoogle ScholarPubMed
Brooks, B.R., Miller, R.G., Swash, M. (2000). World Federation of Neurology Research Group on Motor Neuron Diseases. El Escorial revisited: Revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 1, 293–299.CrossRefGoogle Scholar
Buschke, H. (1973). Selective reminding for analysis of memory and learning. Journal of Verbal Learning and Verbal Behavior, 12, 543–550.CrossRefGoogle Scholar
Carter, C.S., Mintun, M., Cohen, J.D. (1995). Interference and facilitation effects during selective attention: An H215O PET study of Stroop task performance. Neuroimage, 2, 264–272.CrossRefGoogle ScholarPubMed
Cedarbaum, J.M., Stambler, N. (1997). Performance of the Amyotrophic Lateral Sclerosis Functional Rating Scale (ALSFRS) in multicenter clinical trials. Journal of Neurological Sciences, 152, S1–S9.CrossRefGoogle ScholarPubMed
Chari, G., Shaw, P.J., Sahgal, A. (1996). Nonverbal visual attention, but not recognition memory or learning, processes are impaired in motor neuron disease. Neuropsychologia, 34, 377–385.CrossRefGoogle Scholar
Chun, M.M., Golomb, J.D., Turk-Browne, N.B. (2011). A taxonomy of external and internal attention. Annual Review of Psychology, 62, 73–101.CrossRefGoogle ScholarPubMed
Chun, M.M., Turk-Browne, N.B. (2007). Interactions between attention and memory. Current Opinion in Neurobiology, 17, 177–184.CrossRefGoogle ScholarPubMed
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Erlbaum.Google Scholar
Craik, F.I., Tulving, E. (1975). Depth of processing and the retention of words in episodic memory. Journal of Experimental Psychology: General, 104, 268–294.CrossRefGoogle Scholar
Desgranges, B., Baron, J.C., Eustache, E. (1998). The functional neuroanatomy of episodic memory: The role of the frontal lobes, the hippocampal formation, and other areas. Neuroimage, 8, 198–213.CrossRefGoogle ScholarPubMed
Evdokimidis, I., Constantinidis, T.S., Gourtzelidis, P., Smyrnis, N., Zalonis, I., Zis, P.V., Papageorgiou, C. (2002). Frontal lobe dysfunction in amyotrophic lateral sclerosis. Journal of Neurological Sciences, 195, 25–33.CrossRefGoogle ScholarPubMed
Frank, B., Haas, J., Heinze, H.J., Stark, E., Munte, T.F. (1997). Relation of neuropsychological and magnetic resonance findings in amyotrophic lateral sclerosis: Evidence for subgroups. Clinical Neurology and Neurosurgery, 99, 79–86.CrossRefGoogle ScholarPubMed
Gallassi, R., Montagna, P., Ciardulli, C., Lorusso, S., Mussuto, V., Stracciari, A. (1985). Cognitive impairment in motor neuron disease. Acta Neurologica Scandinavica, 71, 480–484.CrossRefGoogle ScholarPubMed
Goldstein, L.H., Atkins, L., Leigh, P.N. (2002). Correlates of quality of life in people with motor neuron disease (MND). Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 3, 123–129.CrossRefGoogle ScholarPubMed
Hanagasi, H.A., Gurvit, I.H., Ermutlu, N., Kaptanoglu, G., Karamursel, S., Idrisoglu, H.A., Demiralp, T. (2002). Cognitive impairment in amyotrophic lateral sclerosis: Evidence from neuropsychological investigation and event-related potentials. Brain Research Cognitive Brain Research, 14, 234–244.CrossRefGoogle ScholarPubMed
Hartikainen, P., Helkala, E.L., Soininen, H., Riekkinen, P. (1993). Cognitive and memory deficits in untreated Parkinson's disease and amyotrophic lateral sclerosis patients: A comparative study. Journal of Neural Transmission. Parkinson's Disease and Dementia Section, 6, 127–137.CrossRefGoogle ScholarPubMed
Iivanainen, M., Laaksonen, R., Niemi, M.-L., Farkkila, M., Bergstrom, L., Mattson, K., Cantell, K. (1985). Memory and psychomotor impairment following high-dose interferon treatment in amyotrophic lateral sclerosis. Acta Neurologica Scandinavica, 52, 475–480.Google Scholar
Iwasaki, Y., Kinoshita, M., Ikeda, K., Takamiya, K., Shiojima, T. (1990). Cognitive impairment in amyotrophic lateral sclerosis and its relation to motor disabilities. Acta Neurologica Scandinavica, 81, 141–143.CrossRefGoogle ScholarPubMed
Kato, S., Hayashi, H., Yagishita, A. (1993). Involvement of the frontotemporal lobe and limbic system in amyotrophic lateral sclerosis: As assessed by serial computed tomography and magnetic resonance imaging. Journal of the Neurological Sciences, 116, 52–58.CrossRefGoogle ScholarPubMed
Kew, J.J., Goldstein, L.H., Leigh, P.N., Abrahams, S., Cosgrave, N., Passingham, R.E., Brooks, D.J. (1993). The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis. A neuropsychological and positron emission tomography study. Brain, 116, 1399–1423.CrossRefGoogle ScholarPubMed
Kilani, M., Micallef, J., Soubrouillard, C., Rey-Lardiller, D., Demattei, C., Dib, M., Blin, O. (2004). A longitudinal study of the evolution of cognitive function and affective state in patients with amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 5, 46–54.CrossRefGoogle ScholarPubMed
Lakerveld, J., Kotchoubey, B., Kübler, A. (2008). Cognitive function in patients with late stage amyotrophic lateral sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 25–29.CrossRefGoogle ScholarPubMed
Levy, B.J., Kuhl, B.A., Wagner, A.D. (2010). The functional neuroimaging of forgetting. In S. Della Sala (Ed.), Forgetting. NY: Psychology Press.Google Scholar
Lezak, M.D., Howieson, D.B., Loring, D.W. (2004). Neuropsychological assessment. New York: Oxford University Press.Google Scholar
Ludolph, A.C., Langen, K.J., Regard, M., Herzog, H., Kemper, B., Kuwert, T., Feinendegen, L. (1992). Frontal lobe function in amyotrophic lateral sclerosis: A neuropsychologic and positron emission tomography study. Acta Neurologica Scandinavica, 85, 81–89.CrossRefGoogle ScholarPubMed
MacDonald, P.A., MacLeod, C.M. (1998). The influence of attention at encoding on direct and indirect remembering. Acta Psychologica, 98, 291–310.CrossRefGoogle ScholarPubMed
Mantovan, M.C., Baggio, L., Dalla Barba, G., Smith, P., Pegoraro, E., Soraru’, G., Angelini, C. (2003). Memory deficits and retrieval processes in ALS. European Journal of Neurology, 10, 221–227.CrossRefGoogle ScholarPubMed
Massman, P.J., Sims, J., Cooke, N., Haverkamp, L.J., Appel, V., Appel, S.H. (1996). Prevalence and correlates of neuropsychological deficits in amyotrophic lateral sclerosis. Journal of Neurology, Neurosurgery, and Psychiatry, 61, 450–455.CrossRefGoogle ScholarPubMed
Moretti, R., Torre, P., Antonello, R.M., Carraro, N., Cazzato, G., Bava, A. (2002). Complex cognitive disruption in motor neuron disease. Dementia and Geriatric Cognitive Disorders, 14, 141–150.CrossRefGoogle ScholarPubMed
Mulligan, N.W. (1998). The role of attention during encoding in implicit and explicit memory. Journal of Experimental Psychology: Learning, Memory, and Cognition, 24, 27–47.Google ScholarPubMed
Nakano, I. (1993). Temporal lobe lesions in amyotrophic lateral sclerosis with or without dementia: A new pathological study. Neuropathology, 13, 215–227.CrossRefGoogle Scholar
Nyberg, L. (2002). Where encoding and retrieval meet in the brain. In L.R. Squire & D.L. Schacter (Eds.), Neuropsychology of memory (3rd ed.). NY: The Guilford Press.Google Scholar
Okamoto, K., Hirai, S., Yamazaki, T., Sun, X.Y., Nakazato, Y. (1991). New ubiquitin-positive intraneuronal inclusions in the extra-motor cortices in patients with amyotrophic lateral sclerosis. Neuroscience Letters, 129, 233–236.CrossRefGoogle ScholarPubMed
Pinkhardt, E.H., Jürgens, R., Becker, W., Molle, M., Born, J., Ludolph, A.C., Schreiber, H. (2008). Signs of impaired selective attention in patients with amyotrophic lateral sclerosis. Journal of Neurology, 255, 532–538.CrossRefGoogle ScholarPubMed
Raaphorst, J., De Visser, M., Linssen, W.H., de Haan, R.J., Schmand, B. (2009). The cognitive profile of amyotrophic lateral sclerosis: A meta-analysis. Amyotrophic Lateral Sclerosis, 29, 1–13.CrossRefGoogle Scholar
Rey, A. (1964). L’ examen clinique en psychologie. Paris: Presses Universitaires de France.Google Scholar
Ringholz, G.M., Appel, S.H., Bradshaw, M., Cooke, N.A., Mosnik, D.M., Schulz, P.E. (2005). Prevalence and patterns of cognitive impairment in sporadic ALS. Neurology, 65, 586–590.CrossRefGoogle ScholarPubMed
Rippon, G.A., Scarmeas, N., Gordon, P.H., Murphy, P.L., Albert, S.M., Mitsumoto, H., Stern, Y. (2006). An observational study of cognitive impairment in amyotrophic lateral sclerosis. Archives of Neurology, 63, 345–352.CrossRefGoogle ScholarPubMed
Rottig, D., Leplow, B., Eger, K., Ludolph, A.C., Graf, M., Zierz, S. (2006). Only subtle cognitive deficits in non-bulbar amyotrophic lateral sclerosis patients. Journal of Neurology, 253, 333–339.CrossRefGoogle ScholarPubMed
Rusin, R., Ridzon, P., Kulist'ak, P., Keller, O., Bartos, A., Buncova, M., Matej, R. (2010). Relationship between ALS and degree of cognitive impairment, markers of neurodegeneration and predictors for poor outcome: A prospective study. European Journal of Neurology, 17, 23–30.CrossRefGoogle Scholar
Russ, M.O., Lanfermann, H., Zanella, F.E. (1995). Validity studies on the Stroop Color-Word Interference Test with functional MRI. Proceedings of the International Society for Magnetic Resonance in Medicine, S1, 24.Google Scholar
Spreen, O., Strauss, E. (1998). A compendium of neuropsychological tests: Administration, norms, and commentary (2nd ed.). NY: Oxford University Press.Google Scholar
Strong, M.J., Grace, G.M., Orange, J.B., Leeper, H.A., Menon, R.S., Aere, C. (1999). A prospective study of cognitive impairment in ALS. Neurology, 53, 1665–1670.CrossRefGoogle ScholarPubMed
Stukovnik, V., Zidar, J., Podnar, S., Repovs, G. (2010). Amyotrophic lateral sclerosis patients show executive impairments on standard neuropsychological measures and an ecologically valid motor-free test of executive functions. Journal of Clinical and Experimental Neuropsychology, 32, 1095–1109.CrossRefGoogle Scholar
Szymanski, K.F., MacLeod, C.M. (1996). Manipulation of attention at study affects an explicit but not an implicit test of memory. Consciousness and Cognition, 5, 165–175.CrossRefGoogle Scholar
Takeda, T., Uchihara, T., Mochizuki, Y., Mizutani, T., Iwata, M. (2007). Memory deficits in amyotrophic lateral sclerosis with dementia and degeneration of the perforant pathway: A clinicopathological study. Consciousness and Cognition, 260, 225–230.Google ScholarPubMed
Trenerry, M.R., Crosson, B., DeBoe, J., Leber, W.R. (1989). Stroop Neuropsychological Screening Test. Odessa, FL: Psychological Assessment Resources.Google Scholar
Tsermentseli, S., Leigh, P.N., Goldstein, L.H. (2012). The anatomy of cognitive impairment in amyotrophic lateral sclerosis: More than frontal lobe dysfunction. Cortex, 48, 166–182.CrossRefGoogle ScholarPubMed
Turner, M.R., Kierman, M.C., Leigh, P.N., Talbot, K. (2009). Biomarkers in amyotrophic lateral sclerosis. Lancet Neurology, 8, 94–109.CrossRefGoogle ScholarPubMed
Turner, M.R., Modo, M. (2010). Advances in the application of MRI to amyotrophic lateral sclerosis. Expert Opinion on Medical Diagnostics, 4, 483–496.CrossRefGoogle ScholarPubMed
Uncapher, M.R., Rugg, M.D. (2009). Selecting for memory? The influence of selective attention on the mnemonic binding of contextual information. The Journal of Neuroscience, 29, 8270–8279.CrossRefGoogle ScholarPubMed
Vanderploeg, R.D., Schinka, J.A., Retzlaff, P. (1994). Relationships between measures of auditory verbal learning and executive functioning. Journal of Clinical and Experimental Neuropsychology, 16, 243–252.CrossRefGoogle ScholarPubMed
Vieregge, P., Wauschkuhn, B., Heberlein, I., Hagenah, J., Verleger, R. (1999). Selective attention is impaired in amyotrophic lateral sclerosis--a study of event-related EEG potentials. Brain Research Cognitive Brain Research, 8, 27–35.CrossRefGoogle ScholarPubMed
Wang, S., Melhem, E.R., Poptani, H., Woo, J.H. (2011). Neuroimaging in amyotrophic lateral sclerosis. Neurotherapeutics, 8, 63–71.CrossRefGoogle ScholarPubMed
Wechsler, D. (1955). Wechsler Adult Intelligence Scale. NY: The Psychological Corporation.Google Scholar
Wightman, G., Anderson, V.E.R., Martin, J., Swash, M., Anderton, B.H., Neary, D., Leigh, P.N. (1992). Hippocampal and neocortical ubiquitin-immunoreactive inclusions in amyotrophic lateral sclerosis with dementia. Neuroscience Letters, 139, 269–274.CrossRefGoogle ScholarPubMed
Wright, M.J., Schmitter-Edgecombe, M. (2011). The impact of verbal memory encoding and consolidation deficits during recovery from moderate-to-severe traumatic brain injury. Journal of Head Trauma and Rehabilitation, 26, 182–191.CrossRefGoogle ScholarPubMed
Wright, M.J., Woo, E., Schmitter-Edgecombe, M., Hinkin, C.H., Miller, E.N., Gooding, A.L. (2009). The item-specific deficit approach to evaluating verbal memory dysfunction: Rationale, psychometrics, and application. Journal of Clinical and Experimental Neuropsychology, 31, 790–802.CrossRefGoogle ScholarPubMed
Zola-Morgan, S., Squire, L.R. (1993). Neuroanatomy of memory. Annual Review of Neuroscience, 16, 547–563.CrossRefGoogle ScholarPubMed