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Current Biology Vol 18 No 24

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farms, these farms are rapidly


being converted to input-intensive
Intact navigation striate pathways account for TN’s
intact navigation skills.
monocultures [2,3]. Thus, it is
imperative to highlight the ecological
skills after bilateral We investigated the residual vision
for locomotion in TN, an unusual
function of shade coffee farms, not loss of striate cortex subject as the only available case in
only in providing refuge for native the literature with selective bilateral
fauna, but also in preserving habitat occipital damage (but see also [1] for
connectivity and gene-flow processes Beatrice de Gelder1,2,*, Marco a report on intact fear conditioning
essential for reforestation by native Tamietto1,3,4, Geert van Boxtel1, in a similar patient). TN suffered the
tree species. Rainer Goebel5, Arash Sahraie6, first stroke that damaged his occipital
Jan van den Stock1, Bernard M.C. cortex unilaterally, and some 36 days
Supplemental Data Stienen1, Lawrence Weiskrantz7 later a second stroke occurred that
Supplemental data are available at http:// and Alan Pegna8 damaged the occipital cortex of
www.current-biology.com/supplemental/
the other hemisphere (Figure 1A).
S0960-9822(08)01496-6
A patient with bilateral damage to He was initially studied by Pegna
Acknowledgments primary visual (striated) cortex has et al. [2] while in hospital in Geneva
This project was supported by the Helen provided the opportunity to assess after his second stroke. These
Olson Brower Fellowship at the University of just what visual capacities are first observations on TN showed
Michigan (to S.J.) and the National Science possible in the absence of geniculo- affective blindsight in response to
Foundation (award DEB 043665 to C.W.D.). striate pathways. Patient TN suffered facial expressions, as indicated
The authors would like to thank John two strokes in succession, lesioning by condition-specific amygdala
Vandermeer for help in the development and each visual cortex in turn and causing activation for emotional expressions
implementation of this project. The authors clinical blindness over his whole visual of fear, anger and joy compared to
would also like to thank the farmers in Nueva field. Functional and anatomical brain neutral. We studied TN behaviorally,
Alemania, Chiapas for the permission to imaging assessments showed that electroencephalographically and with
collect samples on their land. TN completely lacks any functional brain imaging techniques, including
visual cortex. We report here that, diffusion tensor imaging (DTI), in
References
1. Myers, N., Mittermeier, R.A., Mittermeier,
among other retained abilities, he Tilburg and Maastricht.
C.G., da Fonseca, G.A.B., and Kent, J. can successfully navigate down the No active visual cortex could be
(2000). Biodiversity hotspots for conservation extent of a long corridor in which found in TN in response to a range of
priorities. Nature 403, 853–858.
2. Perfecto, I., Rice, R.A., Greenberg, R., and various barriers were placed. A video visual stimuli in a series of imaging
VanderVoort, M.E. (1996). Shade coffee: recording shows him skillfully avoiding sessions, including different sessions
A disappearing refuge for biodiversity.
Bioscience 46, 598–608.
and turning around the blockages. of retinotopic mapping. Because
3. Donald, P.F. (2004). Biodiversity impacts of This demonstrates that extra-striate it was impossible to control his
some agricultural commodity production pathways in humans can sustain fixation, one could not be certain
systems. Conserv. Biol. 18, 17–37.
4. Klein, A.M., Cunningham, S.A., Bos, M., and sophisticated visuo-spatial skills in that absolutely all visual cortex
Steffan-Dewenter, I. (2008). Advances in the absence of perceptual awareness, had been destroyed or inactivated.
pollination ecology from tropical plantation
crops. Ecology 89, 935–943.
akin to what has been previously Nevertheless, it is a highly reasonable
5. Williams-Guillen, K., Perfecto, I., and reported in monkeys. It remains to be surmise that this was so given
Vandermeer, J. (2008). Bats limit insects in a determined which of the several extra- the consistently negative imaging
neotropical agroforestry system. Science
320, 70.
6. Sekercioglu, C.H. (2006). Ecological
significance of bird populations. In Handbook
of the Birds of the World, Volume 11.
J. Del Hoyo, A. Elliott, and D. Christie, eds.
(Barcelona, Lynx Edicions), pp. 15–51.
7. Sezen, U.U., Chazdon, R.L., and Holsinger,
K.E. (2005). Genetic consequences of tropical
second-growth forest regeneration. Science
307, 891.
8. Aldrich, P.R., and Hamrick, J.L. (1998).
Reproductive dominance of pasture trees in
a fragmented tropical forest mosaic. Science
281, 103–105.
9. Luck, G.W., and Daily, G.C. (2003). Tropical
countryside bird assemblages: Richness,
composition, and foraging differ by landscape
context. Ecol. Appl. 13, 235–247.
10. Vekemans, X., and Hardy, O.J. (2004). New
insights from fine-scale spatial genetic
structure analyses in plant populations. Mol.
Ecol. 13, 921–935.

1Department of Ecology and Evolutionary


Biology, University of Michigan, Ann Arbor, Figure 1. Anatomical description of the lesions in TN.
MI 48109, USA. 2University of Michigan (A) T1-weighted MRI (axial view) showing TN’s lesions and confirming bilateral destruction of
Herbarium, 3600 Varsity Drive, Ann Arbor, the visual cortex (Talairach z-coordinates are given; left is left, right is right). (B) Fibers of the
MI 48108-2287, USA. 3Smithsonian Tropical corpus callosum (CC) in TN (view from left-posterior). While seed points were placed in the en-
Research Institute, P.O. Box 0843-03092, tire CC, only fibers originating from the genu and body of the CC were found. In the splenium,
Balboa Ancón, Republic of Panamá. no callosal fibers were detected. Only infero-frontal running fibers could be delineated, which
*E-mail: sjha@umich.edu do not belong to CC.
Magazine
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findings, and it is further supported by witnessed by several colleagues who Supplemental Data
a computer-based perimetry test in applauded spontaneously when he Supplemental data are available at http://
which no sparing was found. completed the course. This was filmed www.current-biology.com/supplemental/
Behaviorally, TN was blind across and is available as a video clip in the S0960-9822(08)01433-4
the whole visual field. He walked Supplemental Data available on-line
like a blind man, using his stick with this issue. Acknowledgments
to track obstacles and requiring There is evidence suggesting that We wish to thank T.N. for his co-operation
guidance by another person when blind or blindfolded sighted subjects and P. Pullens for help in DTI processing.
walking around the various laboratory are able, to some extent, to use the This study was partly supported by a grant
buildings during testing. He was natural auditory obstacle sense to from the SNSF (32-109928) to A.P., a grant
not cognitively impaired except for locate a travel path, although auditory from the EU (FP6-2005-NEST-Path Imp
some mild word- finding difficulty. guidance is notably inferior to visual 043403-COBOL) to B.d.G., by the McDonnell
OCNC to L.W., and by a Veni grant from
Psychophysical tests specifically guidance and deteriorates markedly
NWO (451-07-032) to M.T.
designed to assess the blind fields when small targets are used to define
of subjects with cortical blindness the travel path [8]. Therefore, the
[3,4], including detection of the theoretical possibility that TN was References
1. Hamm, A.O., Weike, A.I., Schupp, H.T., Treig,
presence/absence of big targets in an guided by echolocation abilities from T., Dressel, A., and Kessler, C. (2003). Affective
alternative forced-choice task, proved reflection of sound waves, rather blindsight: intact fear conditioning to a visual
cue in a cortically blind patient. Brain 126,
completely negative; no residual than by unacknowledged visual 267–275.
visual function could be found. He inputs, cannot be totally ruled out. 2. Pegna, A.J., Khateb, A., Lazeyras, F., and
showed some evidence of visuo- Nevertheless, this appears as an Seghier, M.L. (2005). Discriminating emotional
faces without primary visual cortices involves
motor integration in spatially-guided extremely remote possibility in the the right amygdala. Nat. Neurosci. 8, 24–25.
reaching. Furthermore, he was able to present case, as neither TN nor the 3. Sahraie, A., Trevethan, C.T., and MacLeod,
M.J. (2008). Temporal properties of spatial
discriminate the difference between a experimenter following behind him channel of processing in hemianopia.
long rod randomly placed in horizontal emitted any detected sound during Neuropsychologia 46, 879–885.
or non-horizontal positions, with a navigation that might have generated 4. Sahraie, A., Trevethan, C.T., Weiskrantz,
L., Olson, J., MacLeod, M.J., Murray, A.D.,
difference threshold of approximately sound waves reverberation from the Dijkhuizen, R.S., Counsell, C., and Coleman, R.
25°. This, as it happens, was one of objects laying on the floor. Moreover, (2003). Spatial channels of visual processing
in cortical blindness. Eur. J. Neurosci. 18,
the very first behavioral tests that the spatial resolution that can be 1189–1196.
revealed DB’s residual capacities in obtained through any echolocation 5. Weiskrantz, L., Warrington, E.K., Sanders,
informal testing [5,6]. capacity in humans is significantly M.D., and Marshall, J. (1974). Visual capacity
in the hemianopic field following a restricted
The DTI results (carried out by below that necessary to explain TN’s occipital ablation. Brain 97, 709–728.
Rainer Goebel and colleagues in accurate navigation performance 6. Weiskrantz, L. (1986). Blindsight: A Case Study
and Implications (Oxford: Clarendon Press).
Maastricht) showed a severe loss of through small objects, as can be 7. Bridge, H., Thomas, O., Jbabdi, S., and Cowey,
posterior callosal fibers connecting observed in the video [9,10]. A. (2008). Changes in connectivity after visual
the two occipital lobes, as assessed Similar findings to these were cortical brain damage underlie altered visual
function. Brain 131, 1433–1444.
by near-zero fractional anisotropy reported by Humphrey [11] for a 8. Strelow, E.R., and Brabyn, J.A. (1982).
values (Figure 1B). In contrast monkey, ‘Helen’, with bilateral striate Locomotion of the blind controlled by natural
sound cues. Perception 11, 635–640.
to cases of unilateral occipital cortical lesions, which at present 9. Larsen, E., Iyer, N., Lansing, C.R., and Feng, A.
hemianopia, where cross-callosal remain the only antecedents of our (2008). On the minimum audible difference in
processing appears to be important results. Helen successfully avoided direct-to-reverberant energy ratio. J. Acoust.
Soc. Am. 124, 450–461.
in linking an input to the damaged various obstacles in an open-field 10. Voss, P., Lassonde, M., Gougoux, F., Fortin, M.,
hemisphere with the homologous test (as illustrated in a video clip Guillemont, J., and Lepore, F. (2004). Early- and
late-onset blind individuals show supra-normal
brain regions in the intact hemisphere downloadable from the web link: auditory abilities in far-space. Curr. Biol. 14,
[7], in TN the possibility of such cross- http://viperlib.york.ac.uk/login_pop. 1734–1738.
hemispheric support appears to be asp?filename=Helen3.mpg&thumb_ 11. Humphrey, N.K. (1974). Vision in a monkey
without striate cortex: a case study. Perception
lost, not surprisingly given that both of id=2582). The lesion was found not 3, 241–255.
his hemispheres have been damaged. to be absolutely complete in one
In view of these negative results, hemisphere, leading to the surmise 1Cognitive and Affective Neuroscience
we decided to test his residual that there was a small region of Laboratory, Tilburg University, The
visual abilities for locomotion and intact vision in the far periphery of Netherlands. 2Martinos Center for Biomedical
navigation. We constructed a complex the right visual field. This could not Imaging, MGH-HMS, Charlestown, USA.
3Department of Psychology, University
obstacle course consisting of boxes, have accounted for all the varieties
chairs, and so on, arranged randomly of residual visual functions in Helen, of Torino, Italy. 4Institute for Scientific
Interchange (ISI) Foundation, Torino, Italy.
along a long corridor, without any although there perhaps remains 5Department of Neurocognition, Faculty of
person to guide him and with the some ambiguity in this regard for her Psychology, University of Maastricht, The
removal of his walking cane. An obstacle course performance. Given Netherlands. 6Vision Research Laboratories,
experimenter always followed behind the consonance with the animal School of Psychology, University
him during his traversing the course research background and the extreme of Aberdeen, Scotland. 7Department of
in case of a fall or collision, which rarity of cases with complete cortical Experimental Psychology, University
of Oxford, UK. 8Laboratory of Experimental
seemed a real possibility given his blindness in humans, this striking
Neuropsychology, Neuropsychology Unit and
clinical blindness. Astonishingly, he observation will serve as a take-off Department of Neurology, Geneva University
negotiated it perfectly and never point for future studies, when and if Hospitals, Switzerland.
once collided with any obstacle, as other patients will come to light. E-mail: degelder@nmr.mgh.harvard.edu

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