A neural basis for developmental topographic disorientation

Journal of Neuroscience

Volumn 35, Issue 37, 2015, Pages 12954-12969

  Kim, Jiye G ^a   Aminoff, Elissa M ^b   Kastner, Sabine ^a   Behrmann, Marlene ^b  

^a PRINCETON UNIVERSITY   (United States)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Developmental topographic disorientation; Navigation; Parahippocampal place area; Retrosplenial cortex; Scene perception; Transverse occipital sulcus

Indexed keywords

ADULT; ARTICLE; CARD ROTATION TEST; CLINICAL ARTICLE; COGNITIVE DEFECT; CONNECTOME; CONTROLLED STUDY; CORTICAL THICKNESS (BRAIN); DEVELOPMENTAL TOPOGRAPHIC DISORIENTATION; ECHO PLANAR IMAGING; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEADING ORIENTATION TEST; HUMAN; HUMAN EXPERIMENT; MENTAL ROTATION TEST; PAPER FOLDING TEST; PARAHIPPOCAMPAL PLACE AREA; PRIORITY JOURNAL; RECOGNITION; RESTING STATE NETWORK; RETROSPLENIAL CORTEX; SPATIAL MEMORY TEST; TASK PERFORMANCE; TRANSVERSE OCCIPITAL SULCUS; VISUAL ADAPTATION; AGNOSIA; BRAIN MAPPING; DEPTH PERCEPTION; DIFFUSION TENSOR IMAGING; LIMBIC CORTEX; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL LOBE; PATHOLOGY; PATHOPHYSIOLOGY; PATTERN RECOGNITION; PHYSIOLOGY; SPATIAL BEHAVIOR; SPATIAL ORIENTATION;

AGNOSIA; BRAIN MAPPING; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; LIMBIC LOBE; MAGNETIC RESONANCE IMAGING; MIDDLE AGED; OCCIPITAL LOBE; PATTERN RECOGNITION, VISUAL; SPACE PERCEPTION; SPATIAL NAVIGATION; SPATIAL PROCESSING;

EID: 84941781812     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0640-15.2015     Document Type: Article

References (67)

1. Aguirre GK, D’Esposito M (1999) Topographical disorientation: a synthesis and taxonomy. Brain 122:1613–1628. CrossRef Medline
2. Aguirre GK, Zarahn E, D’Esposito M (1998) An area within human ventral cortex sensitive to “building” stimuli: evidence and implications. Neuron 21:373–383. CrossRef Medline
3. Al-Aidroos N, Said CP, Turk-Browne NB (2012) Top-down attention switches coupling between low-level and high-level areas of human visual cortex. Proc Natl Acad Sci U S A 109:14675–14680. CrossRef Medline
4. Arcaro MJ, McMains SA, Singer BD, Kastner S (2009) Retinotopic organization of human ventral visual cortex. J Neurosci 29:10638–10652. CrossRef Medline
5. Avidan G, Hasson U, Malach R, Behrmann M (2005) Detailed exploration of face-related processing in congenital prosopagnosia: 2. Functional neuroimaging findings. J Cogn Neurosci 17:1150–1167. CrossRef Medline
6. Bandettini PA, Jesmanowicz A, Wong EC, Hyde JS (1993) Processing strategies for time-course data sets in functional MRI of the human brain. Magn Reson Med 30:161–173. CrossRef Medline
7. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR Imaging. Magn Reson Med 50:1077–1088. CrossRef Medline
8. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144–155. CrossRef Medline
9. Behrmann M, Kimchi R (2003) What does visual agnosia tell us about perceptual organization and its relationship to object perception? J Exp Psychol Hum Percept Perform 29:19–42. CrossRef Medline
10. Behrmann M, Peterson MA, Moscovitch M, Suzuki S (2006) Independent representation of parts and the relations between them: Evidence from integrative agnosia. J Exp Psychol Hum Percept Perform 32:1169–1184. CrossRef Medline
11. Bianchini F, Incoccia C, Palermo L, Piccardi L, Zompanti L, Sabatini U, Peran P, Guariglia C (2010) Developmental topographical disorientation in a healthy subject. Neuropsychologia 48:1563–1573. CrossRef Medline
12. Bianchini F, Palermo L, Piccardi L, Incoccia C, Nemmi F, Sabatini U, Guariglia C (2014) Where am I? A new case of developmental topographical disorientation. J Neuropsychol 8:107–124. CrossRef Medline
13. Burgess N (2006) Spatial memory: how egocentric and allocentric combine. Trends Cogn Sci 10:551–557. CrossRef Medline
14. Burgess N (2008) Spatial cognition and the brain. Ann N Y Acad Sci 1124: 77–97. CrossRef Medline
15. Cabeza R, Prince SE, Daselaar SM, Greenberg DL, Budde M, Dolcos F, LaBar KS, Rubin DC (2004) Brain activity during episodic retrieval of autobiographical and laboratory events: an fMRI study using a novel photo paradigm. J Cogn Neurosci 16:1583–1594. CrossRef Medline
16. Ciaramelli E, Rosenbaum RS, Solcz S, Levine B, Moscovitch M (2010) Mental space travel: Damage to posterior parietal cortex prevents egocentric navigation and reexperiencing of remote spatial memories. J Exp Psychol Learn Mem Cogn 36:619–634. CrossRef Medline
17. Crawford JR, Howell DC (1998) Regression equations in clinical neuropsychology: an evaluation of statistical methods for comparing predicted and obtained scores. J Clin Exp Neuropsychol 20:755–762. CrossRef Medline
18. Crawford JR, Garthwaite PH, Howell DC, Gray CD (2004) Inferential methods for comparing a single case with a control sample: modified t-tests versus Mycroft et al.’s (2002) modified ANOVA. Cogn Neuropsychol 21:750–755. CrossRef Medline
19. Croxson PL, Johansen-Berg H, Behrens TE, Robson MD, Pinsk MA, Gross CG, Richter W, Richter MC, Kastner S, Rushworth MF (2005) Quantitative investigation of connections of the prefrontal cortex in the human and macaque using probabilistic diffusion tractography. J Neurosci 25: 8854–8866. CrossRef Medline
20. Dilks DD, Julian JB, Paunov AM, Kanwisher N (2013) The occipital place area is causally and selectively involved in scene perception. J Neurosci 33:1331–1336a. CrossRef Medline
21. Duchaine B, Nakayama K (2006) The Cambridge Face Memory Test: Results for neurologically intact individuals and an investigation of its validity using inverted face stimuli and prosopagnosic participants. Neuropsychologia 44:576–585. CrossRef Medline
22. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, Fried I (2003) Cellular networks underlying human spatial navigation. Nature 425:184–188. CrossRef Medline
23. Ekstrom RB, French JW, Harman H, Dermen D (1976) Manual for the kit of factor-referenced cognitive tests. Princeton, NJ: Educational Testing Service.
24. Epstein RA (2008) Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci 12:388–396. CrossRef Medline
25. Epstein RA, Morgan LK (2012) Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis. Neuropsychologia 50:530–543. CrossRef Medline
26. Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601. CrossRef Medline
27. Epstein RA, Higgins JS, Jablonski K, Feiler AM (2007a) Visual scene processing in familiar and unfamiliar environments. J Neurophysiol 97: 3670–3683. CrossRef Medline
28. Epstein RA, Parker WE, Feiler AM (2007b) Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition. J Neurosci 27:6141–6149. CrossRef Medline
29. Epstein RA, Parker WE, Feiler AM (2008) Two kinds of FMRI repetition suppression? Evidence for dissociable neural mechanisms. J Neurophysiol 99:2877–2886. CrossRef Medline
30. Epstein R, Deyoe EA, Press DZ, Rosen AC, Kanwisher N (2001) Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex. Cogn Neuropsychol 18:481–508. CrossRef Medline
31. Epstein R, Graham KS, Downing PE (2003) Viewpoint-specific scene rep-resentations in human parahippocampal cortex. Neuron 37:865–876. CrossRef Medline
32. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355. CrossRef Medline
33. Habib M, Sirigu A (1987) Pure topographical disorientation: a definition and anatomical basis. Cortex 23:73–85. CrossRef Medline
34. Hashimoto R, Tanaka Y, Nakano I (2010) Heading disorientation: A new test and a possible underlying mechanism. Eur Neurol 63:87–93. CrossRef Medline
35. Hasson U, Harel M, Levy I, Malach R (2003) Large-scale mirror-symmetry organization of human occipito-temporal object areas. Neuron 37:1027–1041. CrossRef Medline
36. Hegarty M, Richardson AE, Montello DR, Lovelace K, Subbiah I (2002) Development of a self-report measure of environmental spatial ability. Intelligence 30:425–447. CrossRef
37. Iaria G, Barton JJ (2010) Developmental topographical disorientation: a newly discovered cognitive disorder. Exp Brain Res 206:189–196. CrossRef Medline
38. Iaria G, Bogod N, Fox CJ, Barton JJ (2009) Developmental topographical disorientation: case one. Neuropsychologia 47:30–40. CrossRef Medline
39. Iaria G, Arnold AE, Burles F, Liu I, Slone E, Barclay S, Bech-Hansen TN, Levy RM (2014) Developmental topographic disorientation and decreased hippocampal functional connectivbity. Hippocampus 24:1364–1374. CrossRef Medline
40. Ino T, Inoue Y, Kage M, Hirose S, Kimura T, Fukuyama H (2002) Mental navigation in humans is processed in the anterior bank of the parietooccipital sulcus. Neurosci Lett 322:182–186. Medline
41. Johnson SC (1967) Hierarchical clustering schemes. Psychometrika 32: 241–254. CrossRef Medline
42. Katayama K, Takahashi N, Ogawara K, Hattori T (1999) Pure topographical disorientation due to right posterior cingulate lesion. Cortex 35:279–282. CrossRef Medline
43. Kim JG, Biederman I (2011) Where do objects become scenes? Cereb Cortex 21:1738–1746. CrossRef Medline
44. Kim JG, Biederman I, Lescroart MD, Hayworth KJ (2009) Adaptation to objects in the lateral occipital complex (LOC): Shape or semantics? Vision Res 49:2297–2305. CrossRef Medline
45. Kobayashi Y, Amaral DG (2000) Macaque monkey retrosplenial cortex: I. Three-dimensional and cytoarchitectonic organization. J Comp Neurol 426:339–365. CrossRef Medline
46. Konen CS, Behrmann M, Nishimura M, Kastner S (2011) The functional neuroanatomy of object agnosia: a case study. Neuron 71:49–60. CrossRef Medline
47. Kozhevnikov M, Hegarty M (2001) A dissociation between object manipulation spatial ability and spatial orientation ability. Mem Cognit 29:745–756. CrossRef Medline
48. Kravitz DJ, Saleem KS, Baker CI, Mishkin M (2011) A new neural framework for visuospatial processing. Nat Rev Neurosci 12:217–230. CrossRef Medline
49. Lavenex P, Suzuki WA, Amaral DG (2004) Perirhinal and parahippocampal cortices of the macaque monkey: intrinsic projections and interconnections. J Comp Neurol 472:371–394. Medline
50. Maguire EA (2001) The retrosplenial contribution to human navigation: a review of lesion and neuroimaging findings. Scand J Psychol 42:225–238. CrossRef Medline
51. Marchette SA, Vass LK, Ryan J, Epstein RA (2014) Anchoring the neural compass: coding of local spatial reference frames in human medial parietal lobe. Nat Neurosci 17:1598–1606. CrossRef Medline
52. Mendez MF, Cherrier MM (2003) Agnosia for scenes in topographagnosia. Neuropsychologia 41:1387–1395. CrossRef Medline
53. Norman-Haignere SV, McCarthy G, Chun MM, Turk-Browne NB (2012) Category-selective background connectivity in ventral visual cortex. Cereb Cortex 22:391–402. CrossRef Medline
54. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113. CrossRef Medline
55. Palermo L, Foti F, Ferlazzo F, Guariglia C, Petrosini L (2014) I find my way in a maze but not in my own territory! Navigational processing in developmental topographical disorientation. Neuropsychology 28:135–146. CrossRef Medline
56. Pinsk MA, Arcaro M, Weiner KS, Kalkus JF, Inati SJ, Gross CG, Kastner S (2009) Neural representations of faces and body parts in macaque and human cortex: a comparative fMRI study. J Neurophysiol 101:2581–2600. Medline
57. Podzebenko K, Egan GF, Watson JD (2002) Widespread dorsal stream activation during a parametric mental rotation task, revealed with functional magnetic resonance imaging. Neuroimage 15:547–558. CrossRef Medline
58. Rilling JK, Glasser MF, Preuss TM, Ma X, Zhao T, Hu X, Behrens TE (2008) The evolution of the arcuate fasciculus revealed with comparative DTI. Nat Neurosci 11:426–428. CrossRef Medline
59. Rolls ET, Robertson RG, Georges-François P (1997) Spatial view cells in the primate hippocampus. Eur J Neurosci 9:1789–1794. CrossRef Medline
60. Schneider KA, Richter MC, Kastner S (2004) Retinotopic organization and functional subdivisions of the human lateral geniculate nucleus: a highresolution functional magnetic resonance imaging study. J Neurosci 24: 8975–8985. CrossRef Medline
61. Sholl MJ, Kenny RJ, Della Porta KA (2006) Allocentric-heading recall and its relation to self-reported sense-of-direction. J Exp Psychol Learn Mem Cogn 32:516–533. CrossRef Medline
62. Stark M (1996) Impairment of an egocentric map of locations: implications for perception and action. Cogn Neuropsychol 13:481–524. CrossRef
63. Swisher JD, Halko MA, Merabet LB, McMains SA, Somers DC (2007) Visual topography of human intraparietal sulcus. J Neurosci 27:5326–5337. CrossRef Medline
64. Takahashi N, Kawamura M, Shiota J, Kasahata N, Hirayama K (1997) Pure topographic disorientation due to right retrosplenial lesion. Neurology 49:464–469. CrossRef Medline
65. Ward EJ, Chun MM, Kuhl BA (2013) Repetition suppression and multivoxel pattern similarity differentially track implicit and explicit visual memory. J Neurosci 33:14749–14757. CrossRef Medline
66. Wechsler D (1997) WMS-III: Wechsler memory scale administration and scoring manual, 3rd ed. San Antonio, TX: Psychological Corporation.
67. Whiteley AM, Warrington EK (1978) Selective impairment of topographical memory: a single case study. J Neurol Neurosurg Psychiatry 41:575–578. CrossRef Medline