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The role of the basal ganglia in the control of automatic visuospatial attention

Published online by Cambridge University Press:  08 September 2006

JOANNE FIELDING ,
NELLIE GEORGIOU-KARISTIANIS  and
OWEN WHITE
JOANNE FIELDING
Affiliation:
Experimental Neuropsychology Research Unit, School of Psychology, Psychiatry, and Psychological Medicine, Monash University, Clayton Campus, Victoria, Australia Royal Melbourne Hospital, Department of Neurology, Parkville, Victoria, Australia
NELLIE GEORGIOU-KARISTIANIS
Affiliation:
Experimental Neuropsychology Research Unit, School of Psychology, Psychiatry, and Psychological Medicine, Monash University, Clayton Campus, Victoria, Australia
OWEN WHITE
Affiliation:
Experimental Neuropsychology Research Unit, School of Psychology, Psychiatry, and Psychological Medicine, Monash University, Clayton Campus, Victoria, Australia Royal Melbourne Hospital, Department of Neurology, Parkville, Victoria, Australia
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Abstract

Cognitive impairments in patients with basal ganglia dysfunction are primarily revealed where performance relies on internal, voluntary control processes. Evidence suggests that this also extends to impaired control of more automatic processes, including visuospatial attention. The present study used a non-predictive peripheral cueing paradigm to compare and contrast visuospatial deficits in patients with Parkinson's disease (PD) with those previously revealed in patients with Huntington's disease (HD) (Fielding et al., 2006a). Compared to age-matched controls, both PD and HD patients exhibited increased distractibility or poor fixation, however only PD patients responded erroneously to cue stimuli more frequently than control subjects. All subjects demonstrated initial facilitation for valid versus invalid cues following the shorter stimulus-onset asynchronies (SOAs) and a performance decrement at the longer SOAs (inhibition of return), although there was a clear differentiation between these groups for immediate SOAs. Unlike both control and PD subjects, where IOR manifested between 350 and 1000 msec, IOR was evident as early as 150 msec for HD patients. Further, for PD patients, spatially valid cues resulted in hyper-reflexivity following 150 msec SOAs, with saccadic latencies shorter than those generated in response to un-cued targets. Thus contrasting deficits were revealed in PD and HD, emphasizing the important contribution of the basal ganglia in the control of more automatic behaviors (JINS, 2006, 12, 657–667.)

Keywords

Parkinson's diseaseHuntington's diseasebasal ganglia disorderssaccadesattentioninhibition.
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 12 , Issue 5 , September 2006 , pp. 657 - 667
Copyright
© 2006 The International Neuropsychological Society

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References

REFERENCES

Armstrong, I.T., Chan, F., Riopelle, R.J., & Munoz, D.P. (2002). Control of saccades in Parkinson's disease. Brain and Cognition, 49, 198–201.Google Scholar
Beck, A. & Steer, R.A. (1991). The Beck Depression Inventory (Manual). New York: Psychological Corporation.
Beck, A., Ward, C., Mendelson, M., Mock, J., & Erbaugh, J. (1961). An inventory for measuring depression. Archives of General Psychiatry, 4, 53–63.Google Scholar
Bradshaw, J., Waterfall, M.L., Phillips, J.G., Iansek, R., Mattingley, J.L., & Bradshaw, J.A. (1993). Re-orientation of attention in Parkinson's disease: An extension to the vibrotactile modality. Neuropsychologia, 31, 51–66.Google Scholar
Briand, K.A., Hening, W., Poizner, H., & Sereno, A.B. (2001). Automatic orienting of visuospatial attention in Parkinson's disease. Neuropsychologia, 39, 1240–1249.CrossRefGoogle Scholar
Brown, D.L. & Marsden, C.D. (1990). Cognitive function in Parkinson's disease: From description to theory. Trends in Neuroscience, 13, 21–28.Google Scholar
Corbetta, M., Akbudak, E., Conturo, T.E., Snyder, A.Z., Ollinger, J.M., Drury, H.A., Linenweber, M.R., Petersen, S.E., Raichle, M.E., Van Essen, D.C., & Shulman, G.L. (1998). A common network of functional areas for attention and eye movements. Neuron, 21, 761–773.Google Scholar
Corbetta, M., Kincade, J.M., Ollinger, J.M., McAvoy, M.P., & Shulman, G.L. (2000). Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nature Neuroscience, 3, 292–297.Google Scholar
Corbetta, M., Kincade, J.M., & Shulman, G.L. (2002). Neural systems for visual orienting and their relationships to spatial working memory. Journal of Cognitive Neuroscience, 14, 508–523.Google Scholar
Crawford, T.J., Bennett, D., Lekwuwa, G.U., Shaunak, S., & Deakin, J.F.W. (2002). Cognition and the inhibitory control of saccades in schizophrenia and Parkinson's disease. Progress in Brain Research, 140, 449–466.Google Scholar
Crevits, L. & De Ridder, K. (1997). Disturbed striatoprefrontal mediated visual behaviour in moderate to severe parkinsonian patients. Journal of Neurology, Neurosurgery and Psychiatry, 63, 296–299.Google Scholar
Danziger, S., Fendrich, R., & Rafal, R.D. (1997). Inhibitory tagging of locations in the blind field of hemianopic patients. Consciousness and Cognition, 6, 291–307.Google Scholar
Dorris, M.C., Klein, C., Everling, S., & Munoz, D.P. (2002). Contribution of the primate superior colliculus to inhibition of return. Journal of Cognitive Neuroscience, 14, 1256–1263.Google Scholar
Fielding, J., Georgiou-Karistianis, N., Bradshaw, J., Millist, L., Churchyard, A., & White, O. (2006). Accelerated time-course of inhibition of return in Huntington's disease. Behavioural Brain Research, 166, 211–219.Google Scholar
Filoteo, J.V., Delis, D.C., Demadura, T., Salmon, D.P., Roman, M.J., & Shults, C.W. (1994). Abnormally rapid disengagement of attention to global and local stimulus levels may underlie the visuoperceptual impairments in Parkinson's patients. Neuropsychology, 8, 210–217.Google Scholar
Filoteo, J.V., Delis, D.C., Salmon, D.P., Demadura, T., Roman, M.J., & Schults, C.W. (1997). An examination of the nature of attentional deficits in patients with Parkinson's disease: Evidence from a spatial orienting task. Journal of the International Neuropsychological Society, 3, 337–347.Google Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). Mini-Mental State. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.Google Scholar
Friedrich, F.J., Beck, D., Egly, R., & Rafal, R.D. (1998). Spatial attention deficits in humans: A comparison of superior parietal and temporo-parietal junction lesions. Neuropsychology, 12, 193–207.Google Scholar
Fuentes, L.J. (2004). Inhibitory processing in the attentional networks. In M.I. Posner (Ed.), Cognitive Neuroscience of Attention, (pp. 45–55). New York: Guilford Press.
Georgiou, N., Bradshaw, J.L., Phillips, J.G., Bradshaw, J.A., & Chiu, E. (1995). The Simon effect and attention deficits in Gilles de la Tourette's syndrome and Huntington's disease. Brain, 118(Pt 5), 1305–1318.Google Scholar
Georgiou, N., Bradshaw, J.L., Phillips, J.G., & Chiu, E. (1996). The effect of Huntington's disease and Gilles de la Tourette's syndrome on the ability to hold and shift attention. Neuropsychologia, 34, 843–851.Google Scholar
Gitelman, D., Nobre, A.C., Parrish, T.B., LaBar, K.S., Kim, Y.H., Meyer, J.R., & Mesulam, M. (1999). A large-scale distributed network for covert spatial attention: Further anatomical delineation based on stringent behavioural and cognitive controls. Brain, 122, 1093–1106.Google Scholar
Hafed, Z.M. & Clark, J.J. (2002). Microsaccades as an overt measure of covert attention shifts. Vision Research, 42, 2533–2545.Google Scholar
Hikosaka, O., Matsumura, M., Kojima, J., & Gardiner, T.W. (1993). Role of basal ganglia in initiation and suppression of saccadic eye movements. In N. Mano, I. Hamada, & M.R. DeLong (Eds.), Role of the Cerebellum and the Basal Ganglia in Voluntary Movement, (pp. 213–219). Amsterdam: Excerpta Medica.
Hikosaka, O., Takikawa, Y., & Kawagoe, R. (2000). Role of the basal ganglia in the control of purposive saccadic eye movements. Physiological Reviews, 80, 953–978.Google Scholar
Hopfinger, J.B., Buonocore, M.H., & Mangun, G.R. (2000). The neural mechanisms of top-down attentional control. Nature Neuroscience, 3, 284–291.Google Scholar
Ivory, S.J., Knight, R.G., Longmore, B.E., & Caradoc-Davies, T. (1999). Verbal memory in non-demented patients with idiopathic Parkinson's disease. Neuropsychologia, 37, 817–828.Google Scholar
Josiassen, R.C., Curry, L.M., & Mancall, E.L. (1983). Development of neuropsychological deficits in Huntington's disease. Archives of Neurology, 40, 791–796.Google Scholar
Kaneko, C.R.S. (1996). Effect of obotenic acid lesions of the omnipause neurons on saccadic eye movements in rhesus macaques. Journal of Neurophysiology, 75, 2229–2242.Google Scholar
Kastner, S. & Pinsk, M.A. (2004). Visual attention as a multilevel selection process. Cognitive, Affective, and Behavioral Neuroscience, 4, 483–500.Google Scholar
Kingstone, A., Klein, R.M., Morein-Zamir, S., Hunt, A., Fisk, J., & Maxner, C. (2002). Orienting attention in aging and Parkinson's disease: Distinguishing modes of control. Journal of Clinical & Experimental Neuropsychology, 24, 951–967.Google Scholar
Klein, R.M. (1988). Inhibitory tagging system facilitates visual search. Nature, 334, 430–431.Google Scholar
Kustov, A.A. & Robinson, D.L. (1996). Shared neural control of attentional shifts and eye movements. Nature, 384, 74–77.Google Scholar
Lasker, A.G. & Zee, D.S. (1997). Ocular motor abnormalities in Huntington's disease. Vision Research, 37, 3639–3645.Google Scholar
Lawrence, A.D., Sahakian, B.J., Hodges, J.R., Rosser, A.E., Lange, K.W., & Robbins, T.W. (1996). Executive and mnemonic functions in early Huntington's disease. Brain, 119, 1633–1645.CrossRefGoogle Scholar
Leigh, R.J., Newman, S.A., Folstein, S.E., Lasker, A.G., & Jensen, B.A. (1983). Abnormal ocular motor control in Huntington's disease. Neurology, 33, 1268–1275.Google Scholar
Marsden, C.D. (1984). The pathophysiology of movement disorders. Neurologic Clinics, 2, 435–459.Google Scholar
Mayer, A.R., Seidenberg, M., Dorflinger, J.M., & Rao, S.C. (2004). Event-related fMRI study of exogenous orienting: Supporting evidence for the cortical basis of inhibition of return. Journal of Cognitive Neuroscience, 161, 262–1271.Google Scholar
McAuley, J.H. (2003). The physiological basis of clinical deficits in Parkinson's disease. Progress in Neurobiology, 69, 27–48.Google Scholar
McPherson, S. & Cummings, J.L. (1996). Neuropsychological aspects of Parkinson's disease and parkinsonism. In I. Grant & K.M. Adams (Eds.), Neuropsychological aspects of neuropsychological disorders, (pp. 288–311). New York: Oxford University Press.
Mesulam, M., Nobre, A.C., Kim, Y.H., Parrish, T.B., & Gitelman, D.R. (2001). Heterogeneity of cingulate contributions to spatial attention. NeuroImage, 13, 1065–1072.Google Scholar
Muller, C., Wenger, S., Fertl, L., & E., A. (1994). Initiation of visual-guided random saccades in parkinsonian patients with severe motor fluctuations. Journal of Neural Transmission, 7, 101–108.Google Scholar
Munoz, D.P. (2002). Saccadic eye movements: Overview of neural circuitry. Progress in Brain Research, 140, 89–96.Google Scholar
Munoz, D.P. & Istvan, P.J. (1998). Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. Journal of Neurophysiology, 79, 1193–1209.Google Scholar
Munoz, D.P. & Wurtz, R.H. (1993). Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. Journal of Neurophysiology, 70, 576–589.Google Scholar
Munoz, D.P. & Wurtz, R.H. (1995). Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. Journal of Neurophysiology, 73, 2313–2333.Google Scholar
Nobre, A., Sebestyen, G.N., Gitelman, D.R., Mesulam, M., Frackowiak, R.S., & Frith, C. (1997). Functional localisation of the system for visuospatial attention using positron emission tomography. Brain, 120, 515–533.Google Scholar
Oostenveld, R., Praamstra, P., Stegeman, D.F., & Van Oosterom, A. (2001). Overlap of attention and movement-related activity in lateralised event-related brain potentials. Clinical Neurophysiology, 112, 477–484.Google Scholar
Perry, R.J. & Zeki, S. (2000). The neurology of saccades and covert shifts in spatial attention: An event-related fMRI study. Brain, 123, 2273–2288.CrossRefGoogle Scholar
Poliakoff, E., O'Boyle, D.J., Moore, A.P., McGlone, F.P., Cody, F.W.J., & Spence, C. (2003). Orienting of attention and Parkinson's disease: Tactile inhibition of return and response inhibition. Brain, 126(Pt 9), 2081–2092.Google Scholar
Pollux, P.M. & Robertson, C. (2001). Voluntary and automatic visual spatial shifts of attention in Parkinson's disease: An analysis of costs and benefits. Journal of Clinical & Experimental Neuropsychology, 23, 662–670.Google Scholar
Posner, M.I. (1980). Orienting of attention. Quarterly Journal of Experimental Psychology, 32, 3–25.Google Scholar
Posner, M.I. & Cohen, Y. (1984). Components of visual orienting. In H. Bouma & D.G. Bouwhuis (Eds.), Attention and Performance. New Jersey: Erlbaum.
Posner, M.I. & Petersen, S.E. (1990). The attention system of the human brain. Annual Review of Neuroscience, 13, 25–42.Google Scholar
Posner, M.I., Rafal, R.D., Choate, L.S., & Vaughan, J. (1985). Inhibition of return: Neural basis and function. Cognitive Neuropsychology, 2, 211–228.Google Scholar
Rafal, R.D., Posner, M.I., Friedman, H.H., Inhoff, A.W., & Bernstein, E. (1988). Orienting of visual attention in progressive supranuclear palsy. Brain, 111, 267–280.Google Scholar
Rascol, O., Clanet, M., Montastruc, J.L., Simonetta, M., Soulier-Esteve, M.J., Doyon, B., & Rascol, A. (1989). Abnormal ocular movements in Parkinson's disease: Evidence for involvement of dopaminergic systems. Brain, 112, 1193–1214.Google Scholar
Rascol, O., Sabatini, U., Simonetta-Moreau, M., Montastruc, J.L., Rascol, A., & Clanet, M. (1991). Square wave jerks in Parkinsonian syndromes. Journal of Neurology, Neurosurgery and Psychiatry, 54, 599–602.Google Scholar
Ro, T., Farne, A., & Chang, E. (2003). Inhibition of return and the human frontal eye fields. Experimental Brain Research, 150, 290–296.Google Scholar
Rottach, K.G., Riley, D.E., DiScenna, A.O., Zivotofsky, A.Z., & Leigh, J.R. (1996). Dynamic properties of horizontal and vertical eye movements in parkinsonian syndromes. Annals of Neurology, 39, 368–377.Google Scholar
Sapir, A., Soroker, N., Berger, A., & Nenik, A. (1999). Inhibition of return in spatial attention: Direct evidence for collicular generation. Nature Neuroscience, 2, 1053–1054.Google Scholar
Schrag, A., Jahanshahi, M., & Quin, N. (2000). What contributes to quality of life in patients with Parkinson's disease. Journal of Neurology Neurosurgery and Psychiatry, 69, 308–312.Google Scholar
Seiss, E. & Praamstra, P. (2004). The basal ganglia and inhibitory mechanisms in response selection: Evidence from subliminal priming of motor responses in Parkinson's disease. Brain, 127, 330–339.Google Scholar
Shoulson, I. (1990). Huntington's disease: Cognitive and psychiatric features. Neuropsychiatry, Neuropsychology, and Behavioural Neurology, 3, 15–22.Google Scholar
Small, D.M., Gitelman, D.R., Gregory, M.D., Nobre, A.C., Parrish, T.B., & Mesulam, M. (2003). The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. NeuroImage, 18, 633–641.Google Scholar
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In R.H. Wurtz & M.E. Goldberg (Eds.), The Neurobiology of Saccadic Eye Movements, Vol. 89 (pp. 213–255). Amsterdam: Elsevier.
Spence, C., Lloyd, D., McGlone, F.P., Nicholls, M.E., & Driver, J. (2000). Inhibition of return is supramodal: A demonstration between all possible pairings of vision, touch, and audition. Experiment Brain Research, 134, 42–48.Google Scholar
Sprengelmeyer, R., Lange, H., & Homberg, V. (1995). The pattern of attentional deficits in Huntington's disease. Brain, 118, 145–152.Google Scholar
Tassinari, G., Aglioti, S., Chelazzi, L., Marzi, C.A., & Berlucchi, G. (1987). Distribution in the visual field of the costs of voluntarily allocated attention and of the inhibitory after-effects of covert orienting. Neuropsychologia, 25, 55–71.Google Scholar
Taylor, T.L. & Klein, R.M. (1998). On the causes and effects of inhibition of return. Psychonomic Bulletin & Review, 5, 625–643.Google Scholar
Tipper, S.P., Howard, L.A., & Jackson, S.J. (1997). Selective reaching to grasp: Evidence for distractor interference effects. Vision and Cognition, 4, 1–38.Google Scholar
Tipper, S.P. & Weaver, B. (1998). The medium of attention: Location-based, object-centred, or scene-based? In R.D. Wright (Ed.), Visual Attention, (pp. 77–107). New York: Oxford University Press.
Vonsattel, J.P. (1999). Huntington's disease neuropathology. In A.B. Joseph & R.R. Young (Eds.), Movement Disorders in Neurology and Neuropsychiatry, (pp. 161–170). Massachusetts: Blackwell Science, Inc.
Wascher, E. & Tipper, S.P. (2004). Revealing effects of noninformative spatial cues: An EEG study of inhibition of return. Psychophysiology, 41, 716–728.Google Scholar
Wechsler, D. (1955). Wechsler Adult Intelligence Scale Manual. New York: Psychological Corp.
White, O.B., Saint-Cyr, J.A., & Sharpe, J.A. (1983). Ocular motor deficits in Parkinson's disease. II. Control of the saccadic and smooth pursuit systems. Brain, 106, 571–587.Google Scholar
Wojciulik, E. & Kanwisher, N.G. (1999). The generality of parietal involvement in visual attention. Neuron, 23, 747–764.Google Scholar
Wright, M.J., Burns, R.J., Geffen, G.M., & Geffen, L.B. (1990). Covert orientation of visual attention in Parkinson's disease: An impairment in the maintenance of attention. Neuropsychologia, 28, 151–159.Google Scholar
Yamaguchi, S. & Kobayashi, S. (1998). Contributions of the dopaminergic system to voluntary and automatic orienting of visuospatial attention. Journal of Neuroscience, 18, 1869–1878.Google Scholar