1 Section Neuropsychology, Department of Cognitive Neurology, Hertie-Institute for Clinical Brain Research, University of Tübingen, Tübingen, Germany and 2 INSERM U371 Cerveau et Vision, IFR 19 Institut Fédératif des Neurosciences, Université Claude Bernard LyonI, Lyon, France
Address correspondence to Professor Hans-Otto Karnath, Center of Neurology, University of Tübingen, Hoppe-Seyler-Str. 3, D-72076 Tübingen, Germany. Email: Karnath{at}uni-tuebingen.de.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key Words: brain damage human optic ataxia parietal lobe reaching
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Empirical evidence arguing for this dual stream concept has been derived from neurophysiological work, functional imaging and lesion studies. An important milestone was the observation that stroke patients with parietal lesions may show a specific disorder of co-ordination and accuracy of visually goal-directed hand movements, not related to motor, sensory, visual acuity or visual field disorders. This disorder has been termed optic ataxia. Typically such patients are impaired in reaching and grasping for visual objects with both hands in their contralesional visual field, while they have no problem in reaching when allowed to orient their eyes and head towards the object, i.e. under conditions of central vision.
In a series of cases with missile wound injuries, Ratcliff and Davies-Jones (1972) reported that such patients had skull lesions located in the superior part of the parietal region. In line with these early findings were CT scans of single cases with optic ataxia who showed lesions located in the superior parietal lobule (SPL) (Auerbach and Alexander, 1981
; Ferro, 1984
; Buxbaum and Coslett, 1998
). Perenin and Vighetto (1988)
investigated a series of 10 patients with optic ataxia after unilateral left- or right-sided lesions. The central core of lesion overlap appeared symmetric in both hemispheres. It always included the intraparietal sulcus (IPS) and either the upper part of the inferior parietal lobule (IPL) or more often the medial or the ventral part of the SPL. Based on these early observations many subsequent studies have assumed the SPL (Jeannerod, 1988
; Caminiti et al., 1996
; Rizzolatti et al., 1997
; Milner and Dijkerman, 1998
; Wolpert et al., 1998
; Galletti et al., 1999
, 2003
; Battaglia-Mayer and Caminiti, 2002
; Milner et al., 2003
; Glover, 2003
) and/or the IPS (Pierrot-Deseilligny et al., 1986
; Perenin and Vighetto, 1988
; Milner and Goodale, 1995
; Perenin, 1997
; Milner and Dijkerman, 1998
; Glover, 2003
) as the neural correlate of human optic ataxia.
New tools are now available that provide a more precise lesion localization in humans (for a review, see Rorden and Karnath, 2004). These techniques reduce significantly the uncertainty brought in by the procedures used in previous anatomical studies on optic ataxia, where mainly skull landmarks were taken into consideration (Mazzocchi and Vignolo, 1978
), where only a rather small number of patients was available, and where no direct visual comparison between patients with and without optic ataxia patients via subtraction analysis (cf. Rorden and Karnath, 2004
) was carried out. The present study thus readdressed the question of what the critical lesion site that typically disturbs the control of visually guided reaching in humans is. We investigated the typical lesion location in a large group of 16 unilateral stroke patients with optic ataxia, collected over a time period of 15 years, and compared them with 36 stroke patients without that disorder.
![]() |
Subjects and Methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Patients with optic ataxia perform with large directional errors of the arm and a lack of anticipatory hand shaping, when grasping at objects in peripheral vision (Perenin and Vighetto, 1988). Apart from a few cases where only the hand and finger postural preparation failed (Binkofski et al., 1999
), optic ataxia patients are impaired in both the proximal and distal components of prehension (Perenin and Vighetto, 1988
). The typical pattern of deficit in patients after unilateral brain lesions is gross misreaching in peripheral vision with spared reaching under foveal vision, mostly with the contralesional hand and in the contralesional space (Rondot et al., 1977
; Perenin and Vighetto, 1988
). The majority of these ataxic reaches remain uncorrected. Exceptions occur, for example, when patients get tactile cues on object position while reaching, e.g. when the patient's hand hits the object by chance. In this case, they are able to correct the spatial errors. Sporadically, visually corrected errors are also observed.
In the present study, optic ataxia was assessed by video recordings in two reaching conditions. In the first condition, the patient had to fixate the camera lens in front of him and to grasp for an object (a big pencil) that was presented by the experimenter at various locations in the ipsilesional and then in the contralesional hemispace (Fig. 1a). First the hand ipsilateral and then the hand contralateral to the lesion was tested. In the second condition, instead of fixating the camera lens, the patient had to orient eyes and head towards the object while reaching for it (Fig. 1b). Ten reaches were recorded in each hand/space combination of the two test conditions (peripheral and foveal vision of the target).
|
|
Lesion Analysis
All 52 patients had circumscribed unilateral right or left hemisphere brain lesions due to stroke or surgery in three cases (caverenoma in two, abscess in one). Magnetic resonance imaging (MRI, including diffusion-, T1- and T2-weighted MRI) or computerized tomography (CT) was carried out in each subject, both with high resolution using a slice thickness between 1 and 4 mm for anatomical analysis. The MR scans were oriented along the bicommissural plane; the CT scans along the glabella-inion plane, which is virtually parallel to the later (Tokunaga et al. 1977). The mean time between stroke/surgery and imaging used for the anatomical analysis of lesion location was 60.7 months (SD 75.1). In 11 out of the 16 patients with optic ataxia, MRI images were available, seven in digital format. In these latter cases, the boundary of the lesion was delineated directly on the individual MRI image for every single transversal slice using MRIcro software (Rorden and Brett, 2000
) (http://www.mricro.com). Both the scan and lesion shape were then mapped into stereotaxic space using the spatial normalisation algorithm provided by SPM2 (http://www.fil.ion.ucl.ac.uk/spm/). For determination of the transformation parameters, cost-function masking was employed (Brett et al., 2001
). In those cases where MRI data were not available in digital format or where CT had been performed, MRIcro software was used to map the lesion on transversal slices of the T1-template MRI from the Montreal Neurological Institute (www.bic.mni.mcgill.ca/cgi/icbm_view) that likewise is aligned with stereotaxic space and is distributed with MRIcro. The template scan provides various anatomical landmarks for precisely plotting size and localization of the lesion. Lesions were mapped onto the slices that correspond to Talairach Z-coordinates 24, 16, 8, 0, 8, 12, 16, 20, 24, 28, 32, 36, 40, 44, 48, 52, 56, 60, 64, 68, 72 and 76 mm by using the identical or the closest matching transversal slices of each individual. Automatic three-dimensional rendering of the lesion data was carried out using MRIcro (Rorden and Brett, 2000
).
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
To identify the cortical structures that are commonly damaged in patients with optic ataxia but are typically spared in patients with left or with right hemisphere lesions but no optic ataxia, a first analysis contrasted the optic ataxia patients with control groups A. These groups were comparable with respect to age and the frequency of additional impairments such as paresis, visual field defects, langage disorders, apraxia or spatial neglect. This ensures that the anatomical substrates provoking these latter deficits are represented equally in the group contrasts. We subtracted the superimposed lesions of control groups A (Fig. 3a) from the overlap images of the optic ataxia groups (Fig. 2) revealing percentage overlay plots. Figure 4 illustrates these results and highlights the anatomical structures that were affected more frequently in the patient groups with optic ataxia than in controls A. In both hemispheres, the lesion overlap laterally centered on the IPL, and in the left hemisphere also included the posterior occipito-parietal junction, i.e. the junction between superior occipital gyrus and the SPL (Fig. 4). Via the underlying parietal white matter, the lesion overlap extended medially to the left and the right precuneus, close to the occipito-parietal junction (Fig. 4).
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Functional imaging in healthy human subjects has shown various parietal regions activated in goal-directed movements including both parietal lobules, the IPS and the precuneus, as well as other cortical regions (e.g. Desmurget et al., 2001; Culham et al., 2003
). The large variability in the topography of activations may be partly due to the various tasks requirements. However, when considering the peak of activation in the parieto-occipital region, two main foci can be distinguished. In the early PET studies (Kawashima et al., 1995
; Grafton et al., 1996
; Inoue et al., 1998
; Desmurget et al., 2001
), natural reaching movements were performed with the eyes free to move at the visual target. Among varying foci in these studies a constant observation was activation in the IPS. In the more recent fMRI experiments (DeSouza et al., 2000
; Connolly et al., 2000
, 2003
; Simon et al., 2002
; Medendorp et al., 2003
; Astafiev et al., 2003
), pointing movements were usually carried out in peripheral vision and after a delay of several seconds. In addition to the former, a second focus of activation was observed by most authors in a more dorsal and medial region located in the precuneus, just in front of the parieto-occipital sulcus, which could represent the homologue of the so-called parietal reach region of the monkey (Connolly et al., 2003
). Although most studies have focused on the preparation phase of reaching movements, when the whole time-course of activation was considered, it was observed that the level of activation was even higher during movement execution than preparation (Astafiev et al., 2003
).
Further, several recent studies carried out in monkeys have reported that areas MIP in the medial wall of the intraparietal sulcus and V6A at the junction between medial occipital and precuneate regions take part in processes related to limb action. It was observed that neurons in the parietal reach region, which overlaps areas MIP and V6A, responded preferentially before monkey reaches in peripheral vision (Andersen and Buneo, 2002). Moreover, Galletti et al. (1997)
and Fattori et al. (2001)
have shown that neurons located medial to MIP, in area V6A at the junction between the medial occipital and parietal cortex, are modulated during arm reaching movements. Further studies investigating neuronal activity in areas 5 (PE or PEc), MIP and V6A have hypothesized a role in coding arm movement direction, and in the transformation of sensory input into reference frames that can be used to guide limb action (Kalaska et al., 1983
; Ferraina and Bianchi, 1994
; Lacquaniti et al., 1995
; Batista et al., 1999
; Buneo et al., 2002
; Galletti et al., 2003
).
The present results suggest that these regions are also involved in the control of visually guided reaching in humans. Compatible with the view from both electrophysiology in the monkey and fMRI in normal humans, namely that a homologous parietal reach region is involved in planning (Andersen and Buneo, 2002; Connolly et al., 2003
) and in executing reaching movements (Astafiev et al., 2003
), we found optic ataxia typically associated with a lesion overlap at the hemispheres' medial cortical aspect centering on the precuneus, close to the occipito-parietal junction.
For a greater understanding of the role of areas 5, MIP and V6A in the monkey, it would be interesting to study the consequences of temporary or permanent inactivation. A complete lesion or inactivation of the parietal reach region in the monkey may produce a deficit very similar to optic ataxia in the human. Unfortunately, so far nothing is known about the effects of such extensive damage of this area. However, few studies selectively inactivated areas 5, MIP and/or V6A. The data obtained so far seem to suggest that inactivation of these areas do not provoke severe disruption of visually guided reaching. Cooling of monkey SPL (lateral area 5) failed to provoke misreaching in the natural free gaze condition, but rather gave rise to a restricted disturbance of object manipulation and tactile discrimination with the contralateral hand (Stein, 1978). Instead, misreaching was observed following cooling of the IPL (lateral area 7) (Stein, 1978
). In line with these findings is that lesion of area V6A provoked abnormal wrist and hand rotation (leading to severe disturbance of grasping targets), while misreaching of target positions in peripersonal space was only minimal (Battaglini et al., 2002
). Moreover, Rushworth et al. (1997a
,b
, 1998
) found that although cells in areas 5, MIP and 7b had spatially tuned activity during movements, lesions in these areas did not disrupt visually guided reaching. They found the relation between hand position and limb postural configuration disturbed (Rushworth et al., 1998
). Visual misreaching rather was observed with lesions in the monkey posterior IPL (BA 7a/7ab) and lateral IPS (Rushworth et al., 1997a
). This fits with early cell recording studies showing reach-related activities in the IPL, some of them specific for the contralateral arm and/or a particular direction of space (e.g. Mountcastle et al., 1975
; Leinonen et al., 1979
; see also MacKay, 1992
).
Further studies have observed misreaching in monkeys occurring with lesions of the posterior IPL. In correspondence with our present findings that revealed the center of lesion overlap on the lateral cortical convexity typically at the occipito-parietal junction, they suggest that the posterior IPL is also involved in processes controlling visually guided reaching. Unlike in humans, the defect associated with such lesion occured when the monkeys were free to look at the target, i.e. under natural conditions of central vision. For a few days the animals lose the ability to correctly reach for targets located in peripersonal space, independent of primary visual, motor or sensory disorders (Faugier-Grimaud et al., 1978, 1985
; Stein 1978
; Deuel and Farrar, 1993
; Gallese et al., 1994
; Watson et al., 1994
; Rushworth et al., 1997a
). Longer-lasting misreaching has been observed following lesions of both Brodmann areas 5 and 7, encompassing the IPS (Lamotte and Acuña, 1978
).
In conclusion, our results raise the question what is the function of the largest fraction of human superior parietal lobule if it is not the decisive area for visually guided reaching (in the sense of disrupting this function if lesioned). Functional imaging in healthy human subjects have shown that the SPL is activated in tactile object exploration (Seitz et al., 1991; Binkofski et al., 1999
). SPL activation has further been reported for visuomotor tracking (Grafton et al., 1992
), motor imagery of rotatory hand movements (Wolbers et al., 2003
), changes in visual awareness (probably related to attentional switching mechanisms) (Rees et al., 2002
) and body part localization processing (Felician et al., 2004
). In addition, the SPL may also play a significant role in tactile recognition of objects. Lesions involving the SPL in stroke patients can evoke tactile agnosia, i.e. an inability to recognize everyday objects by tactile exploration (Binkofski et al., 2001
; Bohlhalter et al., 2002
). Moreover, repetitive transcranial magnetic stimulation over SPL has been observed to lead to impaired evaluation of the temporal congruency of pheripheral/central signals associated with self-generated movements (MacDonald and Paus, 2003
).
![]() |
Notes |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Andersen RA, Buneo CA (2002) Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25:189220.[CrossRef][ISI][Medline]
Astafiev SV, Shulman GL, Stanley CM, Snyder AZ, Van Essen DC, Corbetta M (2003) Functional organization of human intraparietal and frontal cortex for attending, looking and pointing. J Neurosci 23:46894699.
Auerbach SH, Alexander MP (1981) Pure agraphia and unilateral optic ataxia associated with a left superior parietal lobule lesion. J Neurol Neurosurg Psychiatry 44:430432.[ISI][Medline]
Battaglia-Mayer A, Caminiti R (2002) Optic ataxia as a result of the breakdown of the global tuning fields of parietal neurones. Brain 125:225237.
Battaglini PP, Mazur A, Galletti C, Skrap M, Brovelli A, Fattori P (2002) Effects of lesions to area V6A in monkeys. Exp Brain Res 144:419422.[CrossRef][ISI][Medline]
Batista AP, Buneo CA, Snyder LH, Andersen RA (1999) Reach plans in eye-centered coordinates. Science 285:257260.
Binkofski F, Buccino G, Stephan KM, Rizzolatti G, Seitz RJ, Freund H-J (1999) A parieto-premotor network for object manipulation: evidence from neuroimaging. Exp Brain Res 128:210213.[CrossRef][ISI][Medline]
Binkofski F, Kunesch E, Classen J, Seitz RJ, Freund H-J (2001) Tactile apraxia: unimodal apractic disorder of tactile object exploration associated with parietal lobe lesions. Brain 124:132144.
Bohlhalter S, Fretz C, Weder B (2002) Hierarchical versus parallel processing in tactile object recognition: a behaviouralneuroanatomical study of aperceptive tactile agnosia. Brain 125:25372548.
Brett M, Leff AP, Rorden C, Ashburner J (2001) Spatial normalization of brain images with focal lesions using cost function masking. Neuroimage 14:486500.[CrossRef][ISI][Medline]
Buneo CA, Jarvis MR, Batista AP, Andersen RA (2002) Direct visuomotor transformations for reaching. Nature 416:632636.[CrossRef][ISI][Medline]
Buxbaum LJ, Coslett HB (1998) Spatio-motor representations in reaching: evidence for subtypes of optic ataxia. Cogn Neuropsychol 15:279312.[CrossRef][ISI]
Caminiti R, Ferraina S, Johnson PB (1996) The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. Cereb Cortex 129:325346.
Connolly JD, Goodale MA, DeSouza JF, Menon RS, Villis T (2000) A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. J Neurophysiol 84:16451655.
Connolly JD, Andersen RA, Goodale MA (2003) FMRI evidence for a parietal reach region in the human brain. Exp Brain Res 153:140145.[CrossRef][ISI][Medline]
Culham J (2003) Human brain imaging reveals a parietal area specialized for grasping. In: Attention and performance. XX. Functional neuroimaging of visual cognition (Kanwisher N, Duncan J, eds), pp. 417438. Oxford: Oxford University Press.
Desmurget M, Grea H, Grethe JS, Prablanc C, Alexander GE, Grafton ST (2001) Functional anatomy of nonvisual feedback loops during reaching: a positron emission tomography study. J Neurosci 21:29192928.
DeSouza JFX, Dukelow SP, Gati JS, Menon RS, Andersen RA, Vilis T (2000) Eye position signal modulates a human parietal pointing region during memory-guided movements. J Neurosci 20:58355840.
Deuel RK, Farrar CA (1993) Stimulus cancellation by macaques with unilateral frontal or parietal lesions. Neuropsychologia 31:2938.[CrossRef][ISI][Medline]
Fattori P, Gamberini M, Kutz DF, Galletti C (2001) Arm-reaching neurons in the parietal area V6A of the macaque monkey. Eur J Neurosci 13:23092313.[CrossRef][ISI][Medline]
Faugier-Grimaud S, Frenois C, Stein DG (1978) Effects of posterior parietal lesions on visually guided behavior in monkeys. Neuropsychologia 16:151168.[CrossRef][ISI][Medline]
Faugier-Grimaud S, Frenois C, Peronnet F (1985) Effects of posterior parietal lesions on visually guided movements in monkeys. Exp Brain Res 59:125138.[ISI][Medline]
Felician O, Romaiguere P, Anton J-L, Nazarian B, Roth M, Poncet M, Roll J-P (2004) The role of human left superior parietal lobule in body part localization. Ann Neurol 55:749751.[CrossRef][ISI][Medline]
Ferraina S, Bianchi L (1994) Posterior parietal cortex: functional properties of neurons in area 5 during an instructed-delay reaching task within different parts of space. Exp Brain Res 99:175178.[ISI][Medline]
Ferro J (1984) Transient inaccuracy in reaching caused by a posterior parietal lobe lesion. J Neurol Neurosurg Psychiatry 47:10161019.[Abstract]
Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5:15251529.[ISI][Medline]
Galletti C, Fattori P, Kutz DF, Battaglini PP (1997) Arm movement-related neurons in the visual area V6A of the macaque superior parietal lobule. Eur J Neurosci 9:410413.[ISI][Medline]
Galletti C, Fattori P, Kutz DF, Gamberini M (1999) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575582.[CrossRef][ISI][Medline]
Galletti C, Kutz DF, Gamberini M, Breveglieri R, Fattori P (2003) Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153:158170.[CrossRef][ISI][Medline]
Glover S (2003) Optic ataxia as a deficit specific to the on-line control of actions. Neurosci Biobehav Rev 27:447456.[CrossRef][ISI][Medline]
Grafton ST, Mazziotta JC, Woods RP, Phelps ME (1992) Human functional anatomy of visually guided finger movements. Brain 115:565587.[Abstract]
Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6:226237.[Abstract]
Hécaen H (1968) Suggestions for a typology of apraxia. In: The reach of mind (Simmel ML, ed.), pp. 3756. New York: Springer.
Hécaen H, Albert ML (1978) Human neuropsychology. New York: Wiley.
Inoue K, Kawashima R, Satoh K, Kinomura S, Goto R, Koyama M, Sugiura M, Ito M, Fukuda H (1998) PET study of pointing with visual feedback of moving hands. J Neurophysiol 79:117125.
Jeannerod M (1988) The neural and behavioural organization of goal-directed movements. Oxford: Oxford University Press.
Kalaska JF, Caminiti R, Georgopoulos AP (1983) Cortical mechanisms related to the direction of two-dimensional arm movements: relations in parietal area 5 and comparison with motor cortex. Exp Brain Res 51:247260.[ISI][Medline]
Kawashima R, Roland PE, O'Sullivan BT (1995) Functional anatomy of reaching and visuomotor learning: a positron emission tomography study. Cereb Cortex 5:111122.[Abstract]
Lacquaniti F, Guigon E, Bianchi L, Ferraina S, Caminiti R (1995) Representing spatial information for limb movement: the role of area 5 in the monkey. Cereb Cortex 5:391409.[Abstract]
Lamotte RH, Acuña C (1978) Defects in accuracy of reaching after removal of posterior parietal cortex in monkeys. Brain Res 139:309326.[CrossRef][ISI][Medline]
Leinonen L, Hyvärinen G, Nyman G, Linnankoski I (1979) Functional properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res 34:299320.[ISI][Medline]
MacDonald PA, Paus T (2003) The role of parietal cortex in awareness of self-generated movements: a transcranial magnetic stimulation study. Cereb Cortex 13:962967.
MacKay WA (1992) Properties of reach-related neuronal activity in cortical area 7A. J Neurophysiol 67:13351345.
Mazzocchi MM, Vignolo LA (1978) Computer assisted tomography in neuropsychological research: a simple procedure for lesion mapping. Cortex 14:136144.[ISI]
Medendorp WP, Goltz HC, Vilis T, Crawford JD (2003) Gaze-centered updating of visual space in human parietal cortex. J Neurosci 23:62096214.
Milner AD, Goodale MA (1995) The visual brain in action. Oxford: Oxford University Press.
Milner AD, Dijkerman HC (1998) Visual processing in the primate parietal lobe. In: Comparative neuropsychology (Milner AD, ed.), pp. 7094. Oxford: Oxford University Press.
Milner AD, Dijkerman HC, McIntosh RD, Rossetti Y, Pisella L (2003) Delayed reaching and grasping in patients with optic ataxia. Prog Brain Res 142:225242.[Medline]
Mountcastle VB, Georgopoulos LA, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871908.
Nieuwenhuys R, Voogd J, van Huijzen C (1988) The human central nervous system, 3rd edn. Berlin: Springer.
Perenin MT (1997) Optic ataxia and unilateral neglect: clinical evidence for dissociable spatial functions in posterior parietal cortex. In: Parietal lobe contributions to orientation in 3D space (Thier P, Karnath H-O, eds), pp. 289308. Heidelberg: Springer.
Perenin MT, Vighetto A (1988) Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111:643674.[Abstract]
Pierrot-Deseilligny C, Gray F, Brunet P (1986) Infarcts of both inferior parietal lobules with impairment of visually guided eye movements, peripheral visual inattention and optic ataxia. Brain 109:8197.[Abstract]
Ratcliff G, Davies-Jones GAB (1972) Defective visual localization in focal brain wounds. Brain 95:4960.[ISI][Medline]
Rees G, Kreiman G, Koch C (2002) Neural correlates of consciousness in humans. Nat Rev Neurosci 3:261270.[CrossRef][ISI][Medline]
Rizzolatti G, Fogassi L, Gallese V (1997) Parietal cortex: from sight to action. Curr Opin Neurobiol 7:562567.[CrossRef][ISI][Medline]
Rondot P, De Recondo J, Ribadeau-Dumas JL (1977) Visuomotor ataxia. Brain 100:355376.[ISI][Medline]
Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12:191200.[ISI][Medline]
Rorden C, Karnath H-O (2004) Using human brain lesions to infer function: a relic from a past era in the fMRI age? Nat Rev Neurosci 5:813819.[ISI][Medline]
Rushworth MFS, Nixon PD, Passingham RE (1997a) Parietal cortex and movements. I. Movement selection and reaching. Exp Brain Res 117:292310.[CrossRef][ISI][Medline]
Rushworth MFS, Nixon PD, Passingham RE (1997b) Parietal cortex and movements. II. Spatial representations. Exp Brain Res 117:311323.[CrossRef][ISI][Medline]
Rushworth MFS, Johansen-Berg H, Young SA (1998) Parietal cortex and spatialpostural transformation during arm movements. J Neurophysiol 79:478482.
Seitz RJ, Roland PE, Bohm C, Greitz T, Stone-Elander S (1991) Somatosensory discrimination of shape: tactile exploration and cerebral activation. Eur J Neurosci 3:481492.[ISI][Medline]
Simon O, Mangin JF, Cohen L, Le Bihan D, Dehaene S (2002) Topograzphycal layout of hand, eye, calculation, and language-related areas in the human parietal lobe. Neuron 33:475487.[CrossRef][ISI][Medline]
Stein J (1978) Effect of parietal lobe cooling on manipulative behaviour in the conscious monkey. In: Active touch (Gordon G, ed.), pp. 7990. Oxford: Pergamon.
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system an approach to cerebral imaging. New York: Thieme.
Tokunaga A, Takase M, Otani K (1977) The glabella-inion line as a baseline for CT scanning of the brain. Neuroradiology 14:6771.[CrossRef][ISI][Medline]
Tzourio-Mazoyer N , Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273289.[CrossRef][ISI][Medline]
Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Analysis of visual behavior (Ingle DJ, Goodale MA, Mansfield RJW, eds), pp. 549586. Cambridge, MA: MIT Press.
Watson RT, Valenstein E, Day A, Heilman KM (1994) Posterior neocortical systems subserving awareness and neglect. Arch Neurol 51:10141021.[Abstract]
Wolbers T, Weiller C, Büchel C (2003) Contralateral coding of imagined body parts in the superior parietal lobe. Cereb Cortex 13:392399.
Wolpert DM, Goodbody SJ, Husain M (1998) Maintaining internal representations: the role of the human superior parietal lobe. Nat Neurosci 1:529533.[CrossRef][ISI][Medline]