Abstract
Progressive supranuclear palsy is often considered a disease of the motor system and is characterised by a profound oculomotor impairment. The oculomotor system is also known to be fundamentally important in cognitive processes such as attention and working memory, but the way in which these functions are affected by PSP is not well understood. In this chapter we outline the pathology and typical presentation of PSP, with a focus on the oculomotor impairment, briefly outline the role of the oculomotor system in spatial cognition and discuss some key studies examining spatial attention and memory in PSP. We then present new data from a study that specifically examined the effect of PSP on visual search. Our results demonstrated a profound impairment of visual search which is most severe for feature search along the vertical axis. These findings are interpreted with respect to the biased-competition theory of attention, and we discuss possible clinical applications of our results.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Awh E, Armstrong KM, Moore T (2006) Visual and oculomotor selection: links, causes and implications for spatial attention. Trends Cogn Sci 10(3):124–130. https://doi.org/10.1016/j.tics.2006.01.001
Ball K, Pearson DG, Smith DT (2013) Oculomotor involvement in spatial working memory is task-specific. Cognition 129(2):439–446. https://doi.org/10.1016/j.cognition.2013.08.006
Barash S, Bracewell RM, Fogassi L, Gnadt JW, Andersen RA (1991) Saccade-related activity in the lateral intraparietal area. I. Temporal properties; comparison with area 7a. J Neurophysiol 66(3):1095–1108. https://doi.org/10.1152/jn.1991.66.3.1095
Bisley JW, Goldberg ME (2010) Attention, intention, and priority in the parietal lobe. Annu Rev Neurosci 33:1–21
Bisley JW, Mirpour K, Arcizet F, Ong WS (2011) The role of the lateral intraparietal area in orienting attention and its implications for visual search. Eur J Neurosci 33(11):1982–1990. https://doi.org/10.1111/j.1460-9568.2011.07700.x
Bower JH, Maraganore DM, McDonnell SK, Rocca WA (1997) Incidence of progressive supranuclear palsy and multiple system atrophy in Olmsted County, Minnesota, 1976 to 1990. Neurology 49(5):1284–1288
Boxer AL, Yu JT, Golbe LI, Litvan I, Lang AE, Hoglinger GU (2017) Advances in progressive supranuclear palsy: new diagnostic criteria, biomarkers, and therapeutic approaches. Lancet Neurol 16(7):552–563. https://doi.org/10.1016/s1474-4422(17)30157-6
Brown RG, Lacomblez L, Landwehrmeyer BG, Bak T, Uttner I, Dubois B et al (2010) Cognitive impairment in patients with multiple system atrophy and progressive supranuclear palsy. Brain 133(Pt 8):2382–2393. https://doi.org/10.1093/brain/awq158
Burrell JR, Hodges JR, Rowe JB (2014) Cognition in corticobasal syndrome and progressive supranuclear palsy: a review. Mov Disord 29(5):684–693. https://doi.org/10.1002/mds.25872
Carrasco M, Ling S, Read S (2004) Attention alters appearance. Nat Neurosci 7(3):308–313
Chambers CD, Stokes MG, Mattingley JB (2004) Modality-specific control of strategic spatial attention in parietal cortex. Neuron 44(6):925–930. https://doi.org/10.1016/j.neuron.2004.12.009
Chen AL, Riley DE, King SA, Joshi AC, Serra A, Liao K et al (2010) The disturbance of gaze in progressive supranuclear palsy: implications for pathogenesis. Front Neurol 1:147. https://doi.org/10.3389/fneur.2010.00147
Chun MM, Wolfe JM (1996) Just say no: how are visual searches terminated when there is no target present? Cogn Psychol 30(1):39–78. https://doi.org/10.1006/cogp.1996.0002
Corbetta M, Shulman GL (2002) Control of goal-directed and stimulus-driven attention in the brain. Nat Neurosci Rev 3:201–215
Corbetta M, Akbudak E, Conturo TE, Snyder AZ, Ollinger JM, Drury HA et al (1998) A common network of functional areas for attention and eye movements. Neuron 21(4):761–773
Cousineau D (2005) Confidence intervals in within-subject designs: a simpler solution to Loftus and Masson’s method. Tutor Quant Methods Psychol 1(1):4–45
Cowey A, Alexander I, Stoerig P (2011) Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans. Brain 134:2149–2157. https://doi.org/10.1093/brain/awr125
Craighero L, Carta A, Fadiga L (2001) Peripheral oculomotor palsy affects orienting of visuospatial attention. Neuroreport 12(15):3283–3286
Craighero L, Nascimben M, Fadiga L (2004) Eye position affects orienting of visuospatial attention. Curr Biol 14(4):331–333
de Haan B, Morgan PS, Rorden C (2008) Covert orienting of attention and overt eye movements activate identical brain regions. Brain Res 1204:102–111. https://doi.org/10.1016/j.brainres.2008.01.105
Desimone R (1998) Visual attention mediated by biased competition in extrastriate visual cortex. Philos Trans R Soc Lond Ser B Biol Sci 353(1373):1245–1255
Deubel H, Schneider WX (1996) Saccade target selection and object recognition: evidence for a common attentional mechanism. Vis Res 36(12):1827–1837
Dickson DW, Ahmed Z, Algom AA, Tsuboi Y, Josephs KA (2010) Neuropathology of variants of progressive supranuclear palsy. Curr Opin Neurol 23(4):394–400. https://doi.org/10.1097/WCO.0b013e32833be924
Dinkin M (2017) Trans-synaptic retrograde degeneration in the human visual system: slow, silent, and real. Curr Neurol Neurosci Rep 17(2):15. https://doi.org/10.1007/s11910-017-0725-2
Fecteau JH, Munoz DP (2006) Salience, relevance, and firing: a priority map for target selection. Trends Cogn Sci 10(8):382–390
Fierro B, Brighina F, Oliveri M, Piazza A, La Bua V, Buffa D, Bisiach E (2000) Contralateral neglect induced by right posterior parietal rTMS in healthy subjects. Neuroreport 11(7):1519–1521
Gabay S, Henik A, Gradstein L (2010) Ocular motor ability and covert attention in patients with Duane Retraction Syndrome. Neuropsychologia 48(10):3102–3109
Gerstenecker A, Mast B, Duff K, Ferman TJ, Litvan I (2013) Executive dysfunction is the primary cognitive impairment in progressive supranuclear palsy. Arch Clin Neuropsychol 28(2):104–113. https://doi.org/10.1093/arclin/acs098
Ghosh BCP, Calder AJ, Peers PV, Lawrence AD, Acosta-Cabronero J, Pereira JM et al (2012) Social cognitive deficits and their neural correlates in progressive supranuclear palsy. Brain 135:2089–2102. https://doi.org/10.1093/brain/aws128
Glasmacher SA, Leigh PN, Saha RA (2017) Predictors of survival in progressive supranuclear palsy and multiple system atrophy: a systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 88(5):402–411. https://doi.org/10.1136/jnnp-2016-314956
Golbe LI (2014) Progressive supranuclear palsy. Semin Neurol 34(2):151–159. https://doi.org/10.1055/s-0034-1381736
Goldberg ME, Bisley J, Powell KD, Gottlieb J, Kusunoki M (2002) The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention. Neurobiol Eye Mov Mol Behav 956:205–215
Grosbras M-H, Paus T (2002) Transcranial magnetic stimulation of the human frontal eye field: effects on visual perception and attention. J Cogn Neurosci 14(7):1109–1120
Hilchey MD, Klein RM, Satel J (2014) Returning to “inhibition of return” by dissociating long-term oculomotor ior from short-term sensory adaptation and other nonoculomotor “inhibitory” cueing effects. J Exp Psychol Hum Percept Perform 40(4):1603–1616. https://doi.org/10.1037/a0036859
Hillyard SA, Vogel EK, Luck SJ (1998) Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. Philos Trans R Soc Lond B Biol Sci 353(1373):1257–1270. https://doi.org/10.1098/rstb.1998.0281
Höglinger GU, Respondek G, Stamelou M, Kurz C, Josephs KA, Lang AE, Movement Disorder Society-endorsed PSP Study Group et al (2017) Clinical diagnosis of progressive supranuclear palsy: the movement disorder society criteria. Mov Disord 32:853–864. https://doi.org/10.1002/mds.26987
Ikkai A, Curtis CE (2011) Common neural mechanisms supporting spatial working memory, attention and motor intention. Neuropsychologia 49(6):1428–1434
Jackson SR, Newport R, Osborne F, Wakely R, Smith DT, Walsh V (2005) Saccade-contingent spatial and temporal errors are absent for saccadic head movements. Cortex 41(2):205–212
Kimura D, Barnett HJM, Burkhart G (1981) The psychological test pattern in progressive supranuclear palsy. Neuropsychologia 19(2):301–306. https://doi.org/10.1016/0028-3932(81)90113-5
Kisvarday ZF, Cowey A, Stoerig P, Somogyi P (1991) Direct and indirect retinal input into degenerated dorsal lateral geniculate-nucleus after striate cortical removal in monkey - implications for residual vision. Exp Brain Res 86(2):271–292
Klein RM (2000) Inhibition of return. Trends Cogn Sci 4(4):138–147
Lane AR, Smith DT, Ellison A, Schenk T (2010) Visual exploration training is no better than attention training for treating hemianopia. Brain 133(6):1717–1728. https://doi.org/10.1093/brain/awq088
Lane AR, Smith DT, Schenk T, Ellison A (2012a) The involvement of posterior parietal cortex and frontal eye fields in spatially primed visual search. Brain Stimul 5(1):11–17
Lane AR, Smith DT, Schenk T, Ellison A (2012b) The involvement of posterior parietal cortex in feature and conjunction visuomotor search. J Cogn Neurosci 23(8):1964–1972. https://doi.org/10.1162/jocn.2010.21576
Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, McKeith I et al (2003) Movement disorders society scientific issues committee report: SIC Task Force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18(5):467–486. https://doi.org/10.1002/mds.10459
Luck SJ, Chelazzi L, Hillyard SA, Desimone R (1997) Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. J Neurophysiol 77(1):24–42
Michalczyk Ł, Paszulewicz J, Bielas J, Wolski P (2018) Is saccade preparation required for inhibition of return (IOR)? Neurosci Lett 665:13–17. https://doi.org/10.1016/j.neulet.2017.11.035
Monza DD, Soliveri PP, Radice DD et al (1998) Cognitive dysfunction and impaired organization of complex motility in degenerative parkinsonian syndromes. Arch Neurol 55(3):372–378. https://doi.org/10.1001/archneur.55.3.372
Morgan EJ, Ball K, Smith DT (2014) The role of the oculomotor system in covert social attention. Atten Percept Psychophys 76(5):1265–1270. https://doi.org/10.3758/s13414-014-0716-1
Muggleton NG, Juan CH, Cowey A, Walsh V (2003) Human frontal eye fields and visual search. J Neurophysiol 89(6):3340–3343
Muller HJ, Rabbitt PMA (1989) Reflexive and voluntary orienting of visual-attention - time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform 15(2):315–330
Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5(3):218–228
Nath U, Ben-Shlomo Y, Thomson RG, Morris HR, Wood NW, Lees AJ, Burn DJ (2001) The prevalence of progressive supranuclear palsy (Steele–Richardson–Olszewski syndrome) in the UK. Brain 124(7):1438–1449. https://doi.org/10.1093/brain/124.7.1438
Nobre AC, Gitelman DR, Dias EC, Mesulam MM (2000) Covert visual spatial orienting and saccades: overlapping neural systems. NeuroImage 11(3):210–216
Pearson DG, Ball K, Smith DT (2014) Oculomotor preparation as a rehearsal mechanism in spatial working memory. Cognition 132(3):416–428. https://doi.org/10.1016/j.cognition.2014.05.006
Pinching AJ, Powell TPS (1971) Ultrastructural features of transneuronal cell degeneration in olfactory system. J Cell Sci 8(1):253
Posner MI (1978) Chronometric explorations of mind. Lawrence Erlbaum Associates, Hillsdale
Posner MI (1980) Orienting of attention. Q J Exp Psychol 32:3–25
Posner MI, Cohen Y (1984) Components of visual orienting. In: Bouma H, Bouwhuis D (eds) Attention and performance X. Lawrence Erlbaum Associates, London, pp 531–556
Posner MI, Cohen Y, Rafal RD (1982) Neural systems control of spatial orienting. Philos Trans R Soc Lond Ser B Biol Sci 298(1089):187–198
Posner MI, Rafal RD, Choate LS, Vaughan J (1985) Inhibition of return - neural basis and function. Cogn Neuropsychol 2(3):211–228
Rafal RD, Posner MI, Friedman JH, Inhoff AW, Bernstein E (1988) Orienting of visual-attention in progressive supranuclear palsy. Brain 111:267–280
Ristic J, Friesen CK, Kingstone A (2002) Are eyes special? It depends on how you look at it. Psychon Bull Rev 9(3):507–513. https://doi.org/10.3758/bf03196306
Rizzolatti G, Riggio L, Sheliga BM (1994) Space and selective attention. Atten Perform 15:231–265
Robbins TW, James M, Owen AM, Lange KW, Lees AJ, Leigh PN et al (1994) Cognitive deficits in progressive supranuclear palsy, Parkinson’s disease, and multiple system atrophy in tests sensitive to frontal lobe dysfunction. J Neurol Neurosurg Psychiatry 57(1):79–88
Schall JD, Cohen JY (2011) The neural basis of saccade target selection. In: Liversedge SP, Gilchrist I, Everling S (eds) The Oxford handbook of eye movements. Oxford University Press, Oxford, pp 357–381
Schrag A, Ben-Shlomo Y, Quinn NP (1999) Prevalence of progressive supranuclear palsy and multiple system atrophy: a cross-sectional study. Lancet 354(9192):1771–1775
Shepherd M, Findlay JM, Hockey RJ (1986) The relationship between eye-movements and spatial attention. Q J Exp Psychol A Hum Exp Psychol 38(3):475–491
Sigurdsson EM (2016) Tau immunotherapy. Neurodegener Dis 16:34–38. https://doi.org/10.1159/000440842
Smith DT, Archibald N (2018) Spatial working memory in Progressive Supranuclear Palsy. Cortex. https://doi.org/10.1016/j.cortex.2018.07.004
Smith DT, Schenk T (2012) The premotor theory of attention: time to move on? Neuropsychologia 50(6):1104–1114
Smith DT, Rorden C, Jackson SR (2004) Exogenous orienting of attention depends upon the ability to execute eye movements. Curr Biol 14(9):792–795
Smith DT, Jackson SR, Rorden C (2005) Transcranial magnetic stimulation of the left human frontal eye fields eliminates the cost of invalid endogenous cues. Neuropsychologia 43(9):1288–1296
Smith DT, Jackson SR, Rorden C (2009a) An intact eye-movement system is not required to generate inhibition of return. J Neuropsychol 3:267–271
Smith DT, Jackson SR, Rorden C (2009b) Repetitive TMS over frontal eye fields disrupts visually cued auditory attention. Brain Stimul 2:81–87
Smith DT, Ball K, Ellison A, Schenk T (2010) Deficits of reflexive attention induced by abduction of the eye. Neuropsychologia 48:1269–1276
Smith DT, Rorden C, Schenk T (2012) Saccade preparation is required for exogenous attention but not endogenous attention or IOR. J Exp Psychol Hum Percept Perform 36(6):1438–1447. https://doi.org/10.1037/a0027794
Smith DT, Ball K, Ellison A (2014) Covert visual search within and beyond the effective oculomotor range. Vis Res 95:11–17. https://doi.org/10.1016/j.visres.2013.12.003
Soliveri P, Monza D, Paridi D, Carella F, Genitrini S, Testa D, Girotti F (2000) Neuropsychological follow up in patients with Parkinson’s disease, striatonigral degeneration-type multisystem atrophy, and progressive supranuclear palsy. J Neurol Neurosurg Psychiat 69(3):313–318. https://doi.org/10.1136/jnnp.69.3.313
Sparks DL, Mays LE (1990) Signal transformations required for the generation of saccadic eye movements. Annu Rev Neurosci 13:309–336
Steele JC, Richardson JC, Olszewski J (1964) Progressive Supranuclear Palsy. A heterogeneous degeneration involving the brain stem, basal ganglia and cerebellum with vertical gaze and pseudobulbar palsy, nuchal dystonia and dementia. Arch Neurol 10:333–359
Thomas NW, Pare M (2007) Temporal processing of saccade targets in parietal cortex area LIP during visual search. J Neurophysiol 97(1):942–947. https://doi.org/10.1152/jn.00413.2006
Tipples J (2002) Eye gaze is not unique: automatic orienting in response to uninformative arrows. Psychon Bull Rev 9(2):314–318
White BJ, Munoz DP (2011) The superior colliculus. In: Liversedge SP, Gilchrist I, Everling S (eds) The Oxford handbook of eye movements. Oxford University Press, Oxford, pp 195–215
Williams DR, de Silva R, Paviour DC, Pittman A, Watt HC, Kilford L et al (2005) Characteristics of two distinct clinical phenotypes in pathologically proven progressive supranuclear palsy: Richardson’s syndrome and PSP-parkinsonism. Brain 128(Pt 6):1247–1258. https://doi.org/10.1093/brain/awh488
Wolfe JM (1994) Guided search 2.0 A revised model of visual search. Psychon Bull Rev 1(2):202–238. https://doi.org/10.3758/bf03200774
Wolfe JM (1998) Visual search. In: Pashler H (ed) Attention. Psychology Press, Hove, pp 13–56
Wolfe JM (2003) Moving towards solutions to some enduring controversies in visual search. Trends Cogn Sci 7(2):70–76
Yeshurun Y, Carrasco M (1998) Attention improves or impairs visual performance by enhancing spatial resolution. Nature 396(6706):72–75
Yoshida K, Hata Y, Kinoshita K, Takashima S, Tanaka K, Nishida N (2017) Incipient progressive supranuclear palsy is more common than expected and may comprise clinicopathological subtypes: a forensic autopsy series. Acta Neuropathol 133(5):809–823. https://doi.org/10.1007/s00401-016-1665-7
Zangemeister WH, Canavan AGM, Hoemberg V (1995) Frontal and parietal transcranial magnetic stimulation (TMS) disturbs programming of saccadic eye-movements. J Neurol Sci 133(1–2):42–52
Zhang J, Rittman T, Nombela C, Fois A, Coyle-Gilchrist I, Barker RA et al (2016) Different decision deficits impair response inhibition in progressive supranuclear palsy and Parkinson’s disease. Brain 139(1):161–173. https://doi.org/10.1093/brain/awv331
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer Nature Switzerland AG
About this chapter
Cite this chapter
Smith, D.T., Archibald, N. (2018). Visual Search in Progressive Supranuclear Palsy. In: Hodgson, T. (eds) Processes of Visuospatial Attention and Working Memory. Current Topics in Behavioral Neurosciences, vol 41. Springer, Cham. https://doi.org/10.1007/7854_2018_72
Download citation
DOI: https://doi.org/10.1007/7854_2018_72
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-31025-7
Online ISBN: 978-3-030-31026-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)