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Research report

fMRI reveals a lower visual field preference for handactions in human superior parieto-occipital cortex(SPOC) and precuneus

Stephanie Rossit a,*, Teresa McAdam b,d, D. Adam Mclean b, Melvyn A. Goodale b,c,d andJody C. Culham b,c,d

a The School of Psychology University of East Anglia Norwich, NR4 7TJ UKb The Brain and Mind Institute, Natural Sciences Centre, University of Western Ontario, London, Ontario, Canadac Department of Psychology, University of Western Ontario, London, Ontario, Canadad Neuroscience Program, University of Western Ontario, London, Ontario, Canada

a r t i c l e i n f o

Article history:

Received 22 May 2012

Reviewed 16 July 2012

Revised 12 October 2012

Accepted 11 December 2012

Action editor Yves Rossetti

Published online 8 January 2013

Keywords:

Grasping

Brain

Vision

Visuomotor control

Parietal lobe

* Corresponding author.E-mail address: rossit.sb@gmail.com (S. R

0010-9452/$ e see front matter ª 2013 Elsevhttp://dx.doi.org/10.1016/j.cortex.2012.12.014

a b s t r a c t

Humans are more efficient when performing actions towards objects presented in the

lower visual field (VF) than in the upper VF. The present study used slow event-related

functional magnetic resonance imaging (fMRI) to examine whether human brain areas

implicated in action would show such VF preferences. Participants were asked to fixate one

of four different positions allowing objects to be presented in the upper left, upper right,

lower left or lower right VF. In some trials they reached to grasp the object with the right

hand while in others they passively viewed the object. Crucially, by manipulating the

fixation position, rather than the position of the objects, the biomechanics of the move-

ments did not differ across conditions. The superior parieto-occipital cortex (SPOC) and the

left precuneus, brain areas implicated in the control of reaching, were significantly more

activated when participants grasped objects presented in the lower VF relative to the upper

VF. Importantly, no such VF preferences were observed in these regions during passive

viewing. This finding fits well with evidence from the macaque neurophysiology that

neurons within visuomotor regions over-represent the lower VF relative to the upper VF

and indicate that the neural responses within these regions may reflect a functional lower

VF advantage during visually-guided actions.

ª 2013 Elsevier Ltd. All rights reserved.

1. Introduction VF in visuomotor control (Danckert and Goodale, 2001; Brown

Humans are more efficient at reaching and grasping stimuli

presented in the lower visual field (VF) than in the upper VF,

suggesting the existence of a functional advantage for the lower

ossit).ier Ltd. All rights reserved

et al., 2005; Khan and Lawrence, 2005; Binsted and Heath,

2005; Krigolson and Heath, 2006; Brownell et al., 2010; Graci,

2011). These findings are consistent with the proposed special-

ization of the lowerVF for analysis and execution of visuomotor

.

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12526

responses (such as grasping and tool manipulation) within

peripersonal space (Previc, 1990; Danckert and Goodale, 2003).

At an anatomical level several brain regions have also been

shown to over-represent the lower VF. In the retina the den-

sity of ganglion cells is approximately 60% greater in the part

of the retina representing the lower VF (superior hemiretina)

versus upper VF (inferior hemiretina) (Curcio et al., 1987;

Curcio and Allen, 1990). In the macaque this asymmetry per-

sists at the level of the dorsal lateral geniculate nucleus

(Schein and de Monasterio, 1987), V1 (Van Essen et al., 1984;

Tootell et al., 1998) and MT (Maunsell and Van Essen, 1987). In

humans, stronger signals for lower VF stimuli have been

found in early visual cortex (Portin and Hari, 1998; Portin et al.,

1999; Liu et al., 2006) and in the lateral occipital cortex (Sayres

and Grill-Spector, 2008; Strother et al., 2010). Nevertheless, to

date, there has been no systematic investigation of VF pref-

erences in human brain regions during visuomotor tasks. One

candidate area that might show a lower VF preference is the

superior parieto-occipital cortex (SPOC), a region implicated in

the guidance of arm movements (de Jong et al., 2001; Astafiev

et al., 2003; Connolly et al., 2003; Prado et al., 2005; Filimon

et al., 2009; Cavina-Pratesi et al., 2010; Gallivan et al., 2011;

Monaco et al., 2011) that preferentially codes targets posi-

tioned in near rather than far space (Quinlan and Culham,

2007; Gallivan et al., 2009). Damage to SPOC is accompanied

by deficits in visuomotor behaviour (Battaglini et al., 2002;

Karnath and Perenin, 2005; Rossit et al., 2009). Interestingly,

single-unit recordings in macaques have demonstrated that

there is a strong bias towards the lower VF in the receptive

fields of neurons in areas V6 (Galletti et al., 1999a) and V6A

(Gamberini et al., 2011), regions thought to correspond to

human SPOC (de Jong et al., 2001; Pitzalis et al., 2006, 2010).

In the current study, we used functional magnetic reso-

nance imaging (fMRI) to examine VF preferences during reach-

to-grasp movements. Critically, by manipulating the locations

where the participants fixated, rather than the position of the

objects, we were able to investigate the effects of where a

stimulus is presented in the VF independently of the move-

ment direction to that stimulus, which remained constant

across conditions. We observed that SPOC and the left pre-

cuneus were significantly more activated when participants

grasped objects presented in the lower relative to the upper VF.

2. Materials and methods

2.1. Participants

Ten participants [3 males; mean age ¼ 27 years, standard

deviation (SD)¼ 5 years] were recruited from the University of

Western Ontario (London, Ontario, Canada) to take part in the

neuroimaging experiment. All participants had taken part in

multiple neuroimaging experiments studying human actions

using the current set-up and were highly experienced at

maintaining fixation. Five of these participants and five new

participants (5 males; age mean ¼ 25 years, SD ¼ 5 years) took

part in an additional behavioural control experiment to

measure the kinematic parameters of the grasping move-

ments in a similar set-up to the one used in the scanner. All

participants had normal or corrected-to-normal vision and

were right-handed according to the Edinburgh Handedness

Inventory (Oldfield, 1971). Informed consent was obtained

before the experiments in accordance with procedures

approved by the University’s Health Sciences Research Ethics

Board and all participants were reimbursed for their time.

2.2. Neuroimaging experiment

2.2.1. Experimental paradigmThe present study measured the blood-oxygenation-level

dependent (BOLD) signal while participants were presented

with objects in different parts of the VF and asked to either

reach-to-grasp them using the right hand or to passively view

them. In order to manipulate the object location in the VF, we

kept the physical object location, and thus the biomechanics

of the actions, constant and varied the location of the fixation

point with respect to the object (Brown et al., 2005). That is,

participants were asked to maintain their gaze on one of four

fixation light-emitting diodes (LEDs; of w.1� of visual angle)

positioned w21� diagonally from the central object (located at

w35 cm from the subject’s nose bridge), such that the object

appeared in the upper left, upper right, lower left or lower

right VF with respect to the fixation LED (Fig. 1C).

To isolate the visual response from the motor execution

response we used a slow event-related paradigm with 26-sec

trials (Fig. 1A), each consisting of three distinct periods: Cue,

Wait and Go. The trial began with a 2-sec Cue period during

which an auditory instruction (“Grasp” or “Look”) was pre-

sented to the participants through headphones and one of the

four fixation LEDs was illuminated, signalling the participant

to make a saccade to that location (for repeated trials at the

same fixation location, the same LED remained illuminated).

Participantswere required tomaintain fixation at this location

for the remainder of the trial. After the Cue period, a Wait

period of fixation in darkness, lasting 12 sec, allowed the BOLD

response from the auditory cue and, in some cases from the

saccade to a new fixation location, to return to baseline. In the

Go period the stimulus was illuminated for 250 msec, cueing

the participants to perform the task. This brief period of object

illumination ensured that actions were performed without

visual feedback (i.e., open loop). During grasping trials, par-

ticipants employed a precision grip (using the index finger and

thumb) to grasp the object along its longest axis (without

lifting the object) with their right hand. During Look trials,

participants simply viewed the illuminated object while

maintaining fixation. After the Go period, a final 10 sec of

darkness/fixation (intertrial interval e ITI) was included to

allow the BOLD response to return to baseline prior to the next

trial. In between trials and in Look trials, participants placed

the right hand at a comfortable location on the chest. In

addition, each run contained two baseline periods (32 sec at

the beginning and 24 sec at the end) of darkness in which

participants fixated on another LED (w.1� of visual angle)

located horizontally w10� to the left of the centrally located

object. The windows in the scanner room were blocked and

the room lights remained off such that, with the exception

of the fixation LED, nothing else in the workspace was visible

to the participant when the illuminator LED was off.

The combination of the two tasks (Grasp and Look) and

four VFs (upper left, upper right, lower left and lower right)

Fig. 1 e Experimental paradigm, set-up and conditions. A) Timing of one event-related trial and experimental conditions

from the participant’s point of view. Participants begin each trial by maintaining fixation on one of four illuminated LEDs

(yellow star) within the fixation frame and by receiving an auditory instruction to perform either a reach-to-grasp action

(“Grasp”) or passive view (“Look”) before presentation of the object stimuli. The fixation light remains illuminated

throughout each trial and participants are instructed to maintain fixation at all times. Instructions are followed by a 12-sec

Wait period and then a Go period initiated by the illumination of the 3D object for 250 msec, cueing participants to perform

the instruction without visual feedback (note that for illustration purposes the participant’s hand is visible in the figure, but

in reality participants were not able to see their hand or the object during the task execution). This is then followed by an ITI

during which the fixation LED may change location as shown. B) Pictures of the set-up from side view and of the set of 3D

objects used. The participant’s head is tilted to permit direct view of the 3D object and fixation. The objects are attached to

the Grasparatus II (Culham et al., 2003), which is placed behind the fixation frame. An illuminator LED is directed towards

the central object and a camera sensitive to visible and infrared light records hand movements. C) Experimental conditions

are shown from participant’s point of view. Note that for illustration purposes the participant’s hand is visible in the figure,

but in reality participants were not able to see their hand or the object during the task execution. The yellow star represents

the location of each fixation LEDs. Note that the 3D objects are always placed in the same location and only fixation varies.

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2527

gave rise to a 2 � 4 design consisting of eight experimental

conditions: Grasp lower left; Grasp upper left; Grasp lower

right; Grasp upper right; Look lower left; Look upper left; Look

lower right; Look upper right (Fig. 1C). Each run consisted of 16

trials, such that each of the eight experimental conditionswas

repeated twice, for a total run duration of w7 min. The eight

trial types were pseudo-randomized within a run and

balanced as much as possible across all runs so that each trial

type was preceded and followed an approximately equal

number of times by every other trial type across the entire

experiment. Each participant performed eight functional runs

(providing a total 16 trial repetitions per condition across the

whole session) and one anatomical scan, yielding a total ses-

sion duration up to 2.5 h (including w45 min of set-up).

2.2.2. Experimental set-up, apparatus and stimuliParticipants lay supine in the magnet with the head tilted

(w20e30�) to allow comfortable viewing of the object without

the use of mirrors (Fig. 1C). Because movements of the

shoulder and upper arm may induce artifacts in the

participant’s data (Culham, 2006), the right upper arm was

immobilized to restrict shoulder movements, but allowed for

full rotation about the elbow and wrist.

Objects were attached with Velcro� to the Grasparatus II

(an MR-compatible pneumatically controlled apparatus for

sequential presentation of three-dimensional stimuli; see

Kroliczak et al., 2008 for full description; Fig. 1B). The Grasp-

aratus II was placed above the participant’s hips within direct

view such that the target object was in the same plane as the

fixation lights (w35 cm). This distance enabled comfortable

grasping from a starting position on the chest. Three sets of

eight objects were placed on Velcro strips, allowing the

experimenter to quickly change the stimuli between runs. In

total we used 24 objects (see Fig. 1B) made from translucent

white plastic, which had constant depth (.6 cm), but varied in

length (from 1.8 to 3.6 cm) and width (from 1.6 to 2.6 cm). Four

red LEDs (w.1� of visual angle) mounted on a black wooden

frame were used as fixation points and were placed in front of

the Grasparatus II (Fig. 1B). The fixation LEDs were positioned

in a square such that each LED was at a visual angle of w21�

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12528

diagonally from the centrally presented object. The fixation

frame had an opening at the centre to allow only one object to

be presented at a time (Fig. 1C). A bright LED (illuminator),

positioned above the participant’s head, was used to briefly

illuminate (250msec) the workspace at the onset of the action

period (Fig. 1B).

The solenoids controlling the air flow to the pneumatic

piston rotating the drum of the Grasparatus II, the auditory

cues, the fixation LEDs and the illuminator LED were

controlled via a custom designed program written in Matlab

(The MathWorks, USA) running on an IBM laptop computer

that, at the beginning of each trial, received a trigger from the

workstation controlling the acquisition of the functional data

by the MRI scanner.

An infrared MR-compatible camera (MRC Systems GmbH),

placed above the participant’s head (Fig. 1B), was used to re-

cord participants actions for each run. The videos of each run

were screened off-line to identify any error trials in which

participants did not perform the instruction correctly (less

that 1% of total trials were classified as errors). Unfortunately

it was not possible to record eye movements because MR-

compatible eye tracking systems cannot monitor gaze in the

head-tilted configuration due to occlusion from the eyelids.

For this reason we only included well-trained and expert fMRI

participants from our lab and repeatedly reminded them

about the importance of keeping fixation on the illuminated

LED. In past experiments in which we have examined fixation

stability outside the scanner, our highly experienced partici-

pants have shown very stable gaze, even in relatively more

demanding conditions such as maintaining vergence at a

distance of 15 cm (Quinlan and Culham, 2007).

2.2.3. Data acquisitionAll imaging was performed at the Robarts Research Institute

(London, Ontario, Canada) using a 3 T Siemens TIM MAGNE-

TOM Trio MRI scanner. We used a combination of parallel

imaging coils to achieve a good signal to noise ratio and to

enable direct viewing without mirrors or occlusion. We tilted

(w20�) the posterior half of the 12-channel receive-only head

coil (6-channels) and suspended a 4-channel receive-only flex

coil over the anterior-superior part of the head (Fig. 1B).

Functional MRI volumes were collected using a T2*-

weighted single-shot gradient-echo echo-planar imaging

(EPI) acquisition sequence [time to repetition

(TR) ¼ 2000 msec, slice thickness ¼ 3.3 mm with no gap, in-

plane resolution ¼ 3.3 mm � 3.3 mm, time to echo

(TE) ¼ 30 msec, field of view ¼ 211 mm � 211 mm, matrix

size ¼ 64 � 64, flip angle ¼ 78�]. Each volume comprised 38

slices angled at w30� caudal tilt with respect to the anterior-

to-posterior commissure (ACePC) line, providing near

whole-brain coverage. The slices were collected in ascending

and interleaved order. During each experimental session, a

T1-weighted anatomical image was collected using a 3D

acquisition sequence (TR ¼ 2300msec, TE ¼ 5.93 msec, field of

view ¼ 256 mm � 240 mm � 192 mm, matrix

size ¼ 256 � 240 � 192, flip angle ¼ 9�, 1 mm isotropic voxels).

2.2.4. Data analysisData were analysed using Brain Voyager QX software package

(Version 2.1, Brain Innovation). For each participant, functional

data from each run were screened for motion and/or magnet

artifacts with the cine-loop animation. Given that our partici-

pants were highly experienced, no abrupt movement artifacts

were detected. Brain Voyager’s motion correction (trilinear/

sinc interpolation) was applied to align each functional volume

for a given participant to the functional volume acquired

closest (in time) to the anatomical volume. In addition, data

were preprocessed with a high-pass filter of 2 cycles per run.

Functional data were superimposed on anatomical brain im-

ages, aligned to the ACePC plane, and transformed into

Talairach space (Talairach and Tournoux, 1988).

We took two separate approaches to analyse the data. First,

we conducted an analysis using a region of interest (ROI)

approach in single subjects for regions that were hypothe-

sized to exhibit increased responsiveness to actions in the

lower VF within the parietal lobe (see below for details). The

ROI approach offers advantages that each area can be identi-

fied in individual participants regardless of variations in ste-

reotaxic location and, moreover, specific areas are not blurred

with adjacent areas due to inter-individual anatomical vari-

ability. For this reason, ROI analyses were applied to data

without spatial smoothing. Second, to investigate other

possible areas that may demonstrate lower VF biases for ac-

tion, we conducted a whole-brain voxelwise analysis using a

random effects general linear model (RFX GLM; see below for

details) on data that were spatially smoothed using a 6-mm

(full-width, half-maximum) Gaussian kernel filter. In both

analyses, 24 predictors were generated, one for each of the

eight experimental conditions at each of the three periods

(Cue, Wait and Go). The predictors were generated by

convolving a two-gamma haemodynamic response function

with a series of boxcar functions representing event durations

(of 2 sec, 12 sec and 2 sec for the three periods, respectively).

The ITI served as baseline and errors in performance were

modelled as predictors of no interest. The datawere processed

using percent signal change transformation. Throughout the

manuscript we report the results regarding the Go period as

the main interest of the paper is exploring the regions acti-

vated during action execution towards objects presented in

different parts of the VF. Nevertheless, we performed addi-

tional ROI and voxelwise analyses upon the Wait period acti-

vation, but these did not reveal any of the effects reported for

the Go phase and thus are not reported here. Perhaps the lack

of effects in the Wait phase is not surprising, given that the

current study was not designed to investigate activation

related to motor preparation: the object was only illuminated

at the beginning of the Go phase and our trial duration did not

allow us to disentangle the activation regarding the eye

movement to the fixation from the activation related to the

motor preparation phase.

2.2.5. ROI selection and analysesFor each participant we used a fixed-effects GLM analysis

(corrected for serial correlations) to identify ROIs located in

SPOC and the anterior intraparietal sulcus (aIPS, an area

strongly implicated in grasping; Binkofski et al., 1998; Murata

et al., 2000; Culham et al., 2003). For all participants, the ROIs

were selected using a selection procedure (adapted from

Valyear and Culham, 2010) that can reproducibly yield regions

of similar size across subjects despite inter-individual

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2529

variations in levels of activation. In this method, the peak

activated voxel (with respect to t-statistic) within a region was

first identified based on a contrast of the Go period for all

Grasp plus all Look trials against the baseline. Importantly,

because all four VFs contributed equally to this contrast, the

criteria to identify ROIs were unbiased and independent from

the criteria later used to evaluate VF effects. The statistical

threshold was set to a determinedminimum (t¼ 2) and a cube

of up to (9 mm)3 ¼ 729 mm3 was selected around that peak

voxel. In both hemispheres, voxel selection was constrained

by anatomical landmarks: aIPS included voxels near the

junction of the anterior portion of the intraparietal sulcus (IPS)

and post-central sulcus; SPOC included voxels at the superior

end of the parieto-occipital sulcus (POS), which separates the

occipital and parietal cortices on the medial surface.

For each ROI from each participant we then extracted the

event-related time course of the experimental runs. Within

a given subject, the mean activation level (% BOLD signal

change) for each experimental condition was computed as

the average of the activation at the peak of the response in

the Go period (i.e., volumes 3 and 4, corresponding to 6 and

8 sec after the object illumination). To compare the activa-

tions across conditions, the mean % BOLD signal levels were

then entered into a repeated-measures analysis of variance

(ANOVA) with task (Grasp and Look), VF across the hori-

zontal meridian (upper and lower), and VF across the ver-

tical meridian (left and right) as within-subject effects. Two-

tailed t-tests were used for post-hoc comparisons and the

problem of multiple comparisons was corrected using the

Bonferroni method ( p < .05). Only significant results are

reported.

2.2.6. Voxelwise analysisThe group data were analysed using an RFX GLM with sepa-

rate predictors for each condition and each subject. In order to

control the problemofmultiple comparisonswe implemented

Brain Voyager’s cluster-level statistical threshold estimator.

In this procedurewe first set the voxelwise threshold at p¼ .01

and then the cluster-wise to p < .001. To investigate lower

versus upper VF effects in action we applied the following

contrast: [(Grasp lower right VFþ Grasp lower left VF)> (Grasp

upper right VF þ Grasp upper left VF)]. Moreover, for

completeness we also investigated right versus left VF effects

in action using the following contrast: [(Grasp lower right

VF þ Grasp upper right VF) > (Grasp lower left VF þ Grasp

upper left VF)]. For each significant area we then extracted the

beta weights for each participant for each condition and again

entered them into a repeated-measures ANOVAwith task and

VF across the vertical and horizontal meridians as within-

subject effects. Post-hoc comparisons were performed with

two-tailed t-tests corrected for multiple comparisons using

the Bonferroni method (p < .05).

2.3. Behavioural control experiment

2.3.1. Experimental set-up, apparatus and stimuliThe purpose of this experimentwas to confirmwhether upper/

lower VF preferences would be observed during actual grasping

of objects presented at the eccentricities used in the neuro-

imaging experiment. To this end, four fixation LEDs were

embedded on a black wooden vertical board (91.5 cm2) atw21�

of diagonal eccentricity from a central position, allowing the

object to be presented in the lower right, lower left, upper left,

and upper right VFs. Note that the behavioural experimentwas

performed under different conditions than the fMRI experi-

ment. While in the scanner, participants grasped objects while

lying supine in the magnet bed, but during the behavioural

experiment participants grasped objects while seated. In

addition, in order to obtain a reliable measure of grip-scaling

abilities we used the same planar rectangular objects as Brown

et al. (2005). The irregularly shaped planar objects used in our

fMRI experiment were not well-suited for this purpose due to

their uneven curvature, which makes it difficult to specify the

graspable dimensions and compare them to grip parameters.

Nevertheless, using Brown et al.’s (2005) objects allowed us to

confirm whether a lower VF preference for grasping was pre-

sent at the eccentricities (w21�) tested in the neuroimaging

experiment. Six white Plexiglas objects (of constant surface

area; thickness ¼ 1 cm) with the following dimensions

(width � height, in cm) were used: 2.4 � 5.0, 2.7 � 4.5, 4.0 � 3.0,

4.8 � 2.5, 3.4 � 3.5 and 6.0 � 2.0. Two of these objects (the 2.0

and 3.5 cm heights) were used for later analysis and were

presented a large number of times. The remaining four objects

served as foils on randomly interleaved catch trials that were

included to reduce practice effects. The back of each object

contained a translucent cube allowing it to be inserted into the

vertical board in front of a centrally positioned LED that was

used to illuminate the object (positioned at the participant’s

line of gaze). All room lights were extinguished and partici-

pants could only see the object when it was illuminated. As in

Brown et al. (2005) participants sat upright with the right hand

resting on a response button embedded into a stand located

between the knees. This button served as a starting position for

each trial. Each participant had three infrared-emitting diodes

(IRED) attached with medical tape to the thumb, index finger

and wrist of the right hand. An Optotrak 3D motion-analysis

system (Northern Digital, Canada) recorded the X, Y and Z po-

sitions of each IRED at a frequency of 100 Hz. Participants also

wore PLATO goggles (Translucent Technologies, Canada) and a

pair of Sony headphones. A custom designed program written

inMatlab (TheMathWorks, USA) was used to control the object

presentation, goggles, fixation, object illumination, head-

phones and recordings.

2.3.2. ProcedureAt the start of each trial, when the participant’s hand was

positioned on the start button, the PLATO goggles were in

translucent configuration, preventing the subject from

viewing the workspace and the Sony headphones played

white noise to occlude sound cues that may have resulted

when the experimenter placed the object. After a ready signal

from the experimenter, the PLATO goggles changed to trans-

parent configuration, the white noise stopped and one of the

four fixation LEDs was illuminated. The subject was given

2 sec to adopt the correct gaze position, fixating on the illu-

minated LED, and was repeatedly asked to maintain fixation

for the full duration of the trial. As in the fMRI experiment,

after the fixation time elapsed the target object was illumi-

nated for 250 msec and participants were instructed to grasp

the object along the vertical axis using the right index finger

perform

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c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12530

and thumb. VF and object size were randomly varied and each

testing session consisted of 8 practice trials and of 80 experi-

mental trials. During the experimental block, the two objects

designated for analysis (the 2.0 and the 3.5 cm heights) were

presented eight times at each of the four VFs, totalling 64 tri-

als. On the remaining 16 trials, which were randomly inter-

leaved within the experimental block, the four foil objects

were presented (once at each of the four VFs). For both the

experimental and foil objects participants were always

instructed to grasp. The experimental session tookw30min to

complete per subject.

2.3.3. Data analysisThe raw data from the IREDs were analysed off-line using

customized software written in LabView (National In-

struments, Newbury, UK). The beginning and end of each

movement was defined using a velocity-based criterion of

40 mm/s (obtained from the wrist IRED). In addition, for each

trial the program also computed the reaction time, move-

ment time, time to peak velocity and deceleration time,

maximum grip aperture (MGA) and time to MGA. Reaction

time was obtained from button release. Movement time was

the total time that took the participant to complete the grasp.

MGAwas defined as the peak Euclidean distance between the

thumb and index finger’s IRED positions. MGA variability was

obtained by averaging the standard deviation of the two

experimental objects for each subject per VF. To measure

grip-scaling efficacy, a linear regression analysis was per-

formed between object size and MGA for each subject sepa-

rately per VF to obtain the r2 and slope values. For

normalization, the r2 values were then converted to a Fisher-

transformed r. All measures were analysed with repeated-

measures ANOVAs with VF across the horizontal meridian

[upper VF (UVF) and lower VF (LVF)] and VF across the vertical

meridian (right and left) as within-subject effects. The

problem of multiple comparisons was corrected using the

Bonferroni method (p < .05).

Table

1eTalairach

coord

inatesandstatisticalresu

ltsforANOVAs

Looktrials)>

base

line].SPOC,su

periorparieto-o

ccipitalco

rtex.

listedandforsim

plicity

isnotprese

nted.

Talairach

coord

inates

Brain

areas

XY

ZTask

Up

Left

SPOC

�11�

4�8

4�

430�

6F (

1,9)[

17.88,p[

.002

F (1,9

RightSPOC

10�

4�8

4�

429�

4F (

1,9)[

7.97,p[

.02

F (1,9

Left

aIPS

�40�

6�4

2�

747�

6F (

1,9)[

66.86,p<

.001

F (1,9

RightaIPS

37�

5�3

9�

746�

6F (

1,9)[

60.38,p<

.001

F (1,9

Significa

ntregionsare

indicatedin

bold.

3. Results of neuroimaging experiment

3.1. ROI analysis

3.1.1. Left and right SPOCA contrast of [(all Grasp trials þ all Look trials) > baseline]

revealed consistent activation in each of the 10 participants at

the superior end of POS bilaterally (see Table 1 for Talairach

coordinates). The location of these clusters is similar to pre-

viously reported activations during reachingmovements (e.g.,

Cavina-Pratesi et al., 2010; Prado et al., 2005). Left and right

SPOC ROIs in each participant are shown in Fig. 2A and C

(respectively) together with the mean % BOLD signal for each

condition. The activation patterns for the eight experimental

conditions were examined with the ANOVA for left and right

SPOC separately (see Table 1 for statistics regarding main ef-

fects and interactions).

3.1.1.1. LEFT SPOC: TASK � VF EFFECTS. As can be seen in Table 1,

in left SPOC there was a significantmain effect of task, in that

more activation was found for the Grasp task than the Look

Fig. 2 e ROI results in SPOC. Location of each subject’s left SPOC (A) and right SPOC (C) ROIs localized with the contrast of

(Grasp D Look) versus baseline. The bar graphs display the mean and standard error of % peak BOLD signal for each

condition in left SPOC (B) and right SPOC (D). A, C, in both hemispheres SPOC was found at the superior end of the POS (pink

solid line).

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2531

task (mean difference in % BOLD signal ¼ .43). Moreover, as

shown in Fig. 2B and Table 1, this main effect of task was

further characterized by a significant interaction between

task and upper/lower VF. Post-hoc comparisons revealed

that grasping objects in the lower VF produced higher acti-

vation than grasping objects in the upper VF [T(9) ¼ 3.2,

p ¼ .01], whereas no such VF effect was found for Look trials

( p¼ .28). Finally, therewas also a significantmain effect of VF

across the vertical meridian (see Table 1) in that for both

Grasp and Look trials there was higher activation for objects

presented in the right VF than in the left VF (mean difference

of % BOLD signal ¼ .14). However, no significant task by left/

Fig. 3 e ROI results in aIPS. A, C, location of each subject’s left aIPS (A) and right aIPS (C) ROIs localized with the contrast of

(Grasp D Look) versus baseline. The bar graphs display the mean and standard error of % peak BOLD signal for each

condition in left aIPS (B) and right aIPS (D). A, C, in both hemispheres aIPS was found at the junction of the IPS (red line) and

the post-central sulcus (yellow line).

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12532

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2533

right VF interaction was observed. Also, the left/right and

upper/lower VF factors did not significantly interact.

3.1.1.2. RIGHT SPOC: TASK � VF EFFECTS. In right SPOC we found a

main effect of task (see Table 1), with higher activation for

Grasp than Look trials (mean difference in% BOLD signal¼ .35).

In addition, as seen in Fig. 2D and Table 1, we also found a

significant interaction between VF across the horizontal me-

ridian and task. In particular, and as observed for left SPOC,

grasping objects in the lower VF produced higher activation

than grasping objects in the upper VF [T(9) ¼ 2.5, p ¼ .04],

whereas no difference was found between lower and upper VF

objects in Look trials (p ¼ .79). Moreover, there was also a main

effect of VF across the vertical meridian, which was further

qualified by a task by left/right VF interaction (see Table 1).

Post-hoc contrasts revealed that grasping objects in the left VF

produced higher activation than grasping objects in the right

VF [T(9) ¼ 3.1, p ¼ .02], whereas no such effect was found for

Look trials (p ¼ .07). No significant interaction was found be-

tween the upper/lower and left/right VFs.

3.1.2. Left and right aIPSA contrast of [(all Grasp trials þ all Look trials) > baseline]

identified a clear focus of activation bilaterally in the aIPS, at

the junction between the IPS and the inferior segment of the

post-central sulcus (see Table 1 for Talairach coordinates).

The locations of these foci are similar to previous imaging

studies involving actions towards 3D stimuli (e.g., Cavina-

Pratesi et al., 2010; Castiello and Begliomini, 2008; Kroliczak

et al., 2007; Culham et al., 2008; Frey et al., 2005). Left and

right aIPS ROIs in each participant are shown in Fig. 3A and C

respectively together with the mean % BOLD signal for each

condition. Having identified left and right aIPS in each

participant we then examined the activation patterns in the

eight experimental conditions with ANOVAs (see Table 1 for

statistics regarding main effects and interactions).

3.1.2.1. LEFT aIPS: TASK EFFECT. In contrast to the results in left

SPOC, no effects of left/right or upper/lower VF or interactions

betweenthemainfactorswere found inleftaIPS.Therewasonly

a very robustmain effect of task (see Fig. 3B andTable 1), in that

grasping produced higher activation than looking (mean dif-

ference of % BOLD signal ¼ .79).

3.1.2.2. RIGHT aIPS: TASK AND VF EFFECTS. For the right aIPS there

wasalsoavery robustmaineffectof task (seeFig. 3DandTable1),

with Grasp trials presenting higher activation than Look trials

(mean difference of % BOLD signal ¼ .44). Moreover, as can be

seen in Table 1, there was also a main effect of VF across the

verticalmeridian, in thatduringbothGraspandLooktrialshigher

activationwas found for objects in the left VFwhen compared to

objects in the rightVF.Themaineffect ofupper/lowerVFwasnot

significant and there were no significant interactions between

upper/lower and left/right VFs.

3.2. Voxelwise analysis

3.2.1. Lower versus upper VF effectsWe then ran a whole-brain RFX GLM analysis comparing

grasping objects presented in the lower VF with grasping

objects in the upper VF [(Grasp lower right VF þ Grasp lower

left VF)> (Grasp upper right VFþGrasp upper left VF)]. As seen

in Fig. 4, the activation map (minimum cluster size of 16

voxels or 432 mm3, p < .001) for this contrast showed three

robust clusters of activation located medially in the parietal

and occipital lobes of the left hemisphere: in SPOC (Talairach

coordinates:X¼�16� 3, Y¼�83� 3, Z¼ 32� 2; Fig. 4A), in the

precuneus (Talairach coordinates: X ¼ �8 � 2, Y ¼ �52 � 3,

Z ¼ 44 � 3; Fig. 4B) and in the anterior cuneus, above the cal-

carine fissure (Talairach coordinates: X ¼ �3 � 3, Y ¼ �74 � 4,

Z ¼ 15 � 3; Fig. 4C).

In line with the ROI results, the beta weights of left SPOC

showed activity dependent on object location within the VF

and task (Fig. 4A). In fact, the ANOVA on the beta weights

revealed a significant interaction between task and upper/

lower VF [F(1,9) ¼ 14.05, p ¼ .005]. Consistent with the contrast

used to select the region, grasping objects in the lower VF

produced higher activation than grasping objects in the upper

VF [T(9) ¼ 6.1, p < .001; non-independent contrast], but criti-

cally no such VF effects were found for Look trials (p ¼ .30).

Moreover, there was also a main effect of VF across the ver-

tical meridian [F(1,9) ¼ 7.69, p ¼ .02] in that during both Grasp

and Look trials right VF objects were associated with higher

activation when compared to left VF objects (mean difference

b ¼ 1.09). No other main effects or interactions were observed

for this region.

The cluster in the left precuneus region (Fig. 4B), only

showed a significant upper/lower VF by task interaction

[F(1,9) ¼ 15.86, p ¼ .003]. In line with the contrast used to select

the region, grasping objects in the lower VF produced higher

activation than grasping objects in the upper VF [T(9) ¼ 4.5,

p ¼ .001; non-independent contrast], whereas importantly no

such upper/lower VF effects were found for Look trials

(p ¼ .26); a result similar to the one obtained in the left SPOC

cluster. No othermain effects and interactions were observed.

Finally, the beta weights of the cluster found in the left

anteriorcuneus,above thecalcarinefissure,alsoshowedhigher

activation for grasping objects in the lowerVF than in theupper

VF (Fig. 4C). However, in contrast to the ANOVA results for left

SPOCandprecuneus, no significant interaction betweenupper/

lower VF and task was found for this cluster. There were only

significantmaineffectsof task [F(1,9)¼5.63,p¼ .04]andofupper/

lower VF [F(1,9) ¼ 6.83, p ¼ .03] with no significant left/right VF

effect andno significant interactions between themain factors.

In particular in this region, Grasp activation was higher than

Lookactivation (meandifferenceb¼ .48) and, forbothGraspand

Look trials, the activationwas higher for lower VF objectswhen

compared with upper VF objects (mean difference b ¼ .30).

Therefore, theresponse inthis regionseemstobemainlydriven

by visual stimulation, in that it is activated when stimuli are

presented in the lowerVF, consistentwith its locationabove the

calcarine fissure.Moreover, a left occipital region located below

the calcarine fissure (Talairach coordinates: X ¼ �15 � 4,

Y ¼ �74 � 4, Z ¼ �12 � 3) was activated when objects were

presented in the upper VF, although this cluster did not survive

cluster correction. This implies that participants successfully

maintainedfixationwhilegrasping, as instructed,as theseearly

visual regions below and above the calcarine fissure responded

according to whether the stimulus was presented in the upper

and lower VF respectively.

Fig. 4 e Group RFX voxelwise contrast of Grasp lower > Grasp upper VF results. Group fMRI activation is shown in orange

on group averaged anatomical slices in coronal, axial and sagittal views for each significant region: left SPOC (A), left

precuneus (B) and left cuneus (C), along with a bar graph of its corresponding beta weight activation (on the right side; error

bars represent standard errors) for each condition.

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12534

3.2.2. Right versus left VF effectsFor completeness we also ran awhole-brain RFX GLM analysis

comparing grasping objects on the right VF with grasping

objects on the left VF [(Grasp lower right VF þ Grasp upper

right VF) > (Grasp lower left VF þ Grasp upper left VF)]. The

activation map (see Fig. 5) showed several robust clusters of

activation (minimum cluster size of 18 voxels or 486 mm3,

p < .001) that depended on whether the grasp was made to-

wards rightward or leftward objects (see Table 2 Talairach

coordinates of each cluster). In line with the ROI analysis

in right SPOC, we found that grasping objects in the left

VF produced higher activation than grasping objects in the

right VF.

In addition, as can be seen in Fig. 5, the parahippocampal

gyrus (PaHG) and cuneus showed a contralateral response: for

each region the activation was present in the left hemisphere

when objects were grasped in the right VF and in the right

hemisphere when objects were grasped in the left VF. Note

that the location of this cuneus activation was posterior to the

POS, but below left SPOC, and superior to the cuneus regions

activated in the previous RFX analysis. Moreover, several

other right-hemisphere regions were also significantly acti-

vated when grasps were made towards left VF objects when

compared to grasps to right VF objects: right middle occipital

gyrus (MOG), right aIPS, right superior parietal lobe (SPL), right

superior frontal gyrus (SFG). Finally, the left supramarginal

gyrus and a region in the left occipital pole showed an ipsi-

lateral response: the activation was significantly higher when

graspswere performed in the left VFwhen compared to grasps

in the right VF.

To further explore these effects, ANOVAs were performed

on the extracted beta weights for each of these regions to test

Fig. 5 e Group RFX voxelwise contrast of Grasp right > Grasp left VF results. A) fMRI activation is shown in orange for

contrast of Grasp right VF objects versus Grasp left VF objects and in blue-to-green for the opposite contrast of Grasp

leftward objects > Grasp rightward objects. Activation is overlaid on group averaged anatomical slices (Talairach

coordinates for each activated region can be found in Table 2). Cn, Cuneus; SPOC, superior parieto-occipital cortex; Occ. pole,

occipital pole. B) The bar graphs display the mean and standard error of beta weight activation for each condition for each

region that showed a significant interaction between the task and left/right or upper/lower VFs (see Table 2 and main text

for statistics).

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2535

Table

2eTalairach

coord

inatesandstatisticalresu

ltsforANOVAsperform

edin

each

bra

inareash

owin

grightversusleftVFeffectsin

theRFXanalysis.

Significa

ntregions

are

indicatedin

bold.Cn,Cuneus;

SPOC,su

periorparieto-o

ccipitalco

rtex;Occ

.pole,occ

ipitalpole.Note

thatth

em

ain

effect

ofrightversusleftVFis

notprese

ntedasth

iswasth

eco

ntrast

use

dto

defineth

ese

regionsandth

us,

notsu

rprisingly,itis

significa

ntforallth

eregionslisted.Also,thein

tera

ctionbetw

eenleft/rightandupper/lower

VFswasnotsignifica

ntforallth

eregionslistedandforsim

plicity

isnotprese

nted.

Talairach

coord

inates

2�

2�

2(G

rasp

/Look�

upper/lowerVF�

right/left

VF)ANOVA

Voxelw

ise

analysis

Brain

areas

XY

ZTask

Upper/lower

VF

Task

�right/left

VF

Task

�upper/lowerVF

Task

�upper/lowerVF�

right/left

VF

Rightgrasp

>

left

grasp

Left

PaHG

�19�

4�5

5�

8.9

�10�

3.1

F(1,9)¼

1.97,p¼

.194

F (1,9)¼

2.44,p¼

.153

F (1,9)¼

1.32,p¼

.279

F (1,9)¼

3.45,p¼

.096

F (1,9)¼

3.64,p¼

.089

Left

Cn

�8.9

�2.7

�80�

2.5

24�

5.6

F (1,9)[

6.11,p[

.035

F (1,9)¼

3.85,p¼

.081

F (1,9)¼

.00,p¼

.983

F (1,9)[

21.26,p[

.001

F (1,9)¼

.08,p¼

.791

Left

grasp

>

rightgrasp

RightPaHG

15�

6�5

9�

10

�5.2

�8.2

F(1,9)¼

1.19,p¼

.304

F (1,9)¼

3.70,p¼

.087

F (1,9)¼

2.07,p¼

.184

F (1,9)¼

2.32,p¼

.162

F (1,9)¼

3.45,p¼

.096

RightCn

13�

5.8

�83�

2.7

25�

2.8

F (1,9)¼

3.19,p¼

.108

F (1,9)¼

.64,p¼

.443

F (1,9)[

6.17,p[

.035

F (1,9)¼

4.00,p¼

.077

F (1,9)¼

1.42,p¼

.263

RightMOG

43�

5.1

�66�

6.4

�.27�

6F (

1,9)[

5.39,p[

.045

F (1,9)¼

1.08,p¼

.325

F (1,9)[

7.49,p[

.023

F (1,9)¼

.26,p¼

.625

F (1,9)¼

.245,p¼

.632

RightSPOC

13�

2.1

�83�

2.4

35�

1.9

F (1,9)¼

3.20,p¼

.107

F (1,9)¼

.04,p¼

.852

F (1,9)[

5.21,p[

.048

F (1,9)[

8.12,p[

.019

F (1,9)¼

1.96,p¼

.195

RightaIPS

43�

2.2

�40�

2.9

41�

2.7

F (1,9)¼

2.66,p¼

.137

F (1,9)¼

.23,p¼

.643

F (1,9)[

8.36,p[

.018

F (1,9)¼

1.44,p¼

.261

F (1,9)¼

1.08,p¼

.326

RightSPL

18�

4.2

�71�

452�

2.7

F (1,9)¼

3.80,p¼

.083

F (1,9)¼

.10,p¼

.765

F (1,9)[

10.17,p[

.011

F (1,9)¼

1.88,p¼

.204

F (1,9)¼

1.14,p¼

.314

RightSFG

28�

3.9

45�

3.5

29�

3.3

F (1,9)¼

.65,p¼

.440

F (1,9)¼

.19,p¼

.671

F (1,9)[

7.29,p[

.024

F (1,9)¼

1.28,p¼

.288

F (1,9)¼

.16,p¼

.703

Left

SMG

�35�

2.1

�43�

2.3

37�

5.1

F (1,9)[

12.64,p[

.006

F (1,9)¼

.08,p¼

.785

F (1,9)[

7.14,p[

.026

F (1,9)¼

.74,p¼

.411

F (1,9)¼

.013,p¼

.911

Left

occ

.

pole

�9.5

�5.4

�92�

4.4

�6.9

�3.6

F (1,9)¼

1.05,p¼

.333

F (1,9)¼

.00,p¼

.997

F (1,9)¼

2.49,p¼

.149

F (1,9)¼

2.32,p¼

.162

F (1,9)¼

.10,p¼

.765

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12536

main effects of task and left/right and upper/lower VF as well

as the interactions between these factors. As can be seen in

Table 2, nomain effect of upper/lower VFwas found for all any

of the activated regions, but there was a significant main ef-

fect of task in the left cuneus, right middle occipital and left

supramarginal gyrus. Post-hoc tests revealed that these re-

gions Grasp activation was higher than Look activation (mean

difference b: cuneus ¼ .55; MOG ¼ .26; supramarginal

gyrus ¼ .68). Moreover, this analysis revealed that several re-

gions showed activity dependent on the task performed and

VF in which the object was presented (see Table 2). Regarding

the task by left/right VF interaction, post-hoc tests revealed

that several regions were significantly more activated when

participants performed grasps towards objects presented in

the left VF when compared to the right VF [right cuneus:

T(9) ¼ 4.8, p ¼ .001; right MOG: T(9) ¼ 5.1, p ¼ .001; right SPOC:

T(9) ¼ 3.6, p ¼ .006; right aIPS: T(9) ¼ 4.3, p ¼ .002; left supra-

marginal gyrus: T(9) ¼ 3.6, p¼ .006; right SPL: T(9) ¼ 4.9, p¼ .001;

right SFG: T(9)¼ 4.3, p¼ .002], whereas no such left/right effects

were observed for Look trials (right cuneus: p¼ .22; right MOG:

p ¼ .24; right SPOC: p ¼ .31; right aIPS: p ¼ .62; left supra-

marginal gyrus: p ¼ .70; right SPL: p ¼ .92; right SFG: p ¼ .12).

Moreover, the PaHG responded to contralateral stimuli

regardless of task (see Fig. 5A and Table 2). This pattern of

lateralized responses can be taken as an indication that our

participants generally maintained fixation throughout.

In addition, concerning the task by upper/lower VF inter-

action, as can be seen in Table 2, right SPOC showed a sig-

nificant task by VF interaction, similarly to our previous

analysis. Post-hoc tests revealed that grasping objects pre-

sented in the lower VF produced higher activation than look-

ing at objects in the lower VF [T(9) ¼ 2.6, p ¼ .03], whereas no

such VF differences between tasks were found for objects

presented in the upper VF (p ¼ .40). Moreover, another sig-

nificant task by upper/lower VF interaction was also found in

the left cuneus region and post-hoc tests revealed that there

was higher activation for grasping objects in the lower VF than

in the upper VF [T(9)¼ 3.3, p¼ .009], whereas no such VF effects

were found for Look trials (p ¼ .76).

4. Results of behavioural control experiment

Importantly, the control behavioural experiment demon-

strated that reaction time was statistically indistinguishable

across all conditions (for descriptive statistics see Table 3)

suggesting no differences in object detection or task difficulty.

In terms of grip scaling, we found that MGA variability was

significantly decreased when objects were presented in the

lower VF when compared to when objects were presented in

the upper VF [F(1,9) ¼ 6.04, p ¼ .04; see Table 2]. Moreover, the

relationship between object size and MGA was stronger for

objects in the lower VFwhen compared to objects presented in

the upper VF [Fisher-transformed r: F(1,9) ¼ 19.64, p ¼ .002;

slope: F(1,9) ¼ 13.46, p ¼ .005; see Table 3]. Crucially, however,

no significant effects were found in the time toMGA (see Table

3), indicating no differences inmovement planning across the

VFs. In fact, in terms of timing, the only significant effect was

found for movement time, in that there was significant

interaction between upper/lower VFs and right/left VFs

Table 3 e Mean and standard error (in brackets) for all dependent variables analysed in the behavioural control experimentper stimulus position.

Variable Stimulus position

Lower left Upper left Lower right Upper right

MGA variability (mm) 4.0 (.3) 4.5 (.4) 4.2 (.5) 5.4 (.7)

Fisher-transformed r 1.3 (.1) 1.0 (.1) 1.3 (.1) .9 (.1)

Slope 12.6 (1.4) 9.5 (1.2) 12.6 (1.1) 9.3 (.8)

Reaction time (ms) 382.3 (81.7) 388.8 (90.9) 408.7 (86.9) 402.4 (51.5)

Movement time (ms) 764.1 (59.7) 749.0 (58.2) 758.5 (60.2) 803.3 (64.1)

Time to peak velocity (ms) 266.6 (21.1) 265.9 (24.4) 262.1 (23.2) 265.7 (22.6)

Deceleration time (ms) 497.5 (41.4) 483.1 (38.6) 496.4 (42.6) 537.6 (44.5)

Time to MGA (ms) 524.7 (49.1) 512.6 (53.2) 518.6 (49.9) 523.3 (51.1)

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2537

[F(1,9) ¼ 10.05, p ¼ .01; see Table 3]. Post-hoc tests revealed that

grasping movements made with the right hand were faster

when objects were presented in the right lower VF versus the

right upper VF (mean difference ¼ �44.9 msec, p < .05),

whereas no such upper/lower VF effects were found when

objects were presented on the left VF (mean

difference ¼ �15.1 msec).

Taken together, these findings suggest that the increased

activation found for grasping objects in the lower VF is

accompanied by a more accurate grip scaling rather than a

faster performance.

5. Discussion

For the first time we show that the response of human brain

regions involved in visuomotor control is modulated by the

retinal location of a stimulus within the VF during hand ac-

tions but not passive viewing. In particular, we demonstrate

that SPOC and left precuneus are more active when partici-

pants grasp objects presented in the lower VF than in the

upper VF.

5.1. VF preferences for action in the human brain

The current results complement previous findings that SPOC

and left precuneus are activated during the preparation and

execution of arm movements (Astafiev et al., 2003; Connolly

et al., 2003; Prado et al., 2005; Pellijeff et al., 2006; Beurze

et al., 2007; Filimon et al., 2009; Cavina-Pratesi et al., 2010;

Gallivan et al., 2011; Monaco et al., 2011) and that lesions to

these regions are associated with visuomotor deficits in both

humans (Karnath and Perenin, 2005; Rossit et al., 2009) and

monkeys (Battaglini et al., 2002). Interestingly, both SPOC and

the precuneus have been shown to demonstrate stronger

activation for lower VF stimuli within arm’s reach compared

to stimuli located beyond reach, even when no action is

required (Gallivan et al., 2009). One parsimonious suggestion

then is that SPOC activation is strongest for stimuli within the

region of space in which one typically acts e objects within

reachable spacewithin the lower VF. One difference is that we

find a preference (for the lower VF) only when the subject is

performing an action while Gallivan et al. found a preference

(for reachable objects) even during passive viewing, when no

action occurred. One possible reason for this discrepancymay

be that different factors inform distance [including vergence,

to which SPOC is sensitive, even without an action task

(Quinlan and Culham, 2007), and binocular disparity] and

retinal position (which can be determined solely from

monocular cues). Perhaps the distance cues are strong enough

to evoke responses even when no action occurs, while the

retinal position cues are only relevant when an action is

planned. Regardless of these differences, the common

conclusion is that the visuomotor system is specialized for

processing visual information within the space where actions

most frequently occur. The preference of the visuomotor

system for acting in the lower VF may reflect the fact that, in

our everyday life, the control of skilled hand actions requires

processing of visual information that is more often present in

the lower than in the upper VF (e.g., Graziano et al., 2004). In

fact, our behavioural control experiment indicated that par-

ticipants demonstrated better grip scaling in the lower VF

than in the upper VF in line with previous studies (e.g.,

Danckert and Goodale, 2001; Brown et al., 2005).

Importantly, these differences cannot be simply explained

by low-level differences in movement parameters. Specif-

ically, although the retinal location of the object varied, its

position with respect to the subject’s hand and body, and thus

the movement biomechanics, remained constant across

conditions. Furthermore, no lower VF preferences were

observed in either SPOC or precuneus during passive viewing,

suggesting that our findings were not purely visually-driven.

Similarly, because the action was performed in open loop

we can also rule out the possibility that these activations are

merely due to visual feedback of the moving arm. In addition,

it is also unlikely that our results are due to any distortion in

the perception or detection of the targets in either VF as tar-

gets subtended the same visual angle in both fields and in the

control behavioural experiment the reaction times and times

to MGA did not differ across conditions (albeit the fMRI and

the behavioural studies were performed under different con-

ditions, with different spatial relations between head, hand,

and grasped object, see Methods for specific details).

Furthermore, eye movements cannot fully account for the

effects reported here. If our well-trained expert fMRI subjects

had failed to maintain fixation and instead foveated the tar-

gets, then this presumably would have eliminated any VF

differences. Insteadwe found that the response of early visual

and parahippocampal regions responded according towhere a

stimulus was in the VF regardless of the task performed. In

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 12538

particular, separate clusters above and below the calcarine

fissure responded to stimuli presented in the lower and upper

VF respectively. Moreover, the left PaHG was activated when

stimuli were presented on the right VF whereas the opposite

was true in the right PaHG. Therefore, wewould argue that our

results indicate that regions involved in visuomotor control,

such as SPOC and left precuneus, are specialized for pro-

cessing information in the lower VF specifically in the context

of object-directed actions. This conclusion fits well with the

proposal that the lower VF is specialized for the analysis and

execution of responses (such as grasping and tool manipula-

tion) within peripersonal space (Previc, 1990; Danckert and

Goodale, 2003). Whether this lower VF preference for action

in visuomotor regions can also arise during the motor plan-

ning phase, before the action is executed, deserves further

investigation.

Several studies have reported the existence of VF prefer-

ences in the context of attentional tasks. Interestingly, Handy

et al. (2003) reported that the P1, an early visual event-related

potential component thought to reflect spatial attention, was

larger when drawings of tools were presented in the right and

lower VFs than in the left and upper VFs, even when those

objects were irrelevant to the task requirements. Critically,

the same effect was not observed for non-tool stimuli sug-

gesting that this effect was driven by action-related affor-

dances and not general attention. Using event-related fMRI,

they then found that premotor and parietal cortices were

activated only when tools were presented on the right VF, but

not left VF. The authors conclude that graspable objects cap-

ture attention to their location facilitating visuomotor control.

Therefore, an alternative or complementary explanation is

that attention modulates the activity in SPOC and left pre-

cuneus, thus driving the lower VF bias during hand actions. In

line with this, several studies have reported that the lower VF

has better attentional resolution than the upper VF (e.g., He

et al., 1996; Rubin et al., 1996; Ellison and Walsh, 2000; Talgar

and Carrasco, 2002; for review see Danckert and Goodale,

2003). We did not include an attentional control task

because it may have distorted the nature of processing within

parietal cortex. Nevertheless, we do not believe that atten-

tional confounds can account for the observed results as we

did not find a lower VF preference specific to grasping in re-

gions within the frontoparietal attentional network (e.g.,

Corbetta et al., 2008), but rather only in SPOC and precuneus.

In fact, regions within this attentional network (including

aIPS, frontal eye fields, posterior IPS and a region at the

junction between the IPS and the transverse occipital sulcus)

have been recently shown to present a lower VF preference for

stationary spatial orienting tasks and an upper visual prefer-

ence during visual search tasks (Kraft et al., 2011). In contrast

to these findings, we did not observe any significant VF pref-

erences in any of these regions, including the aIPS, suggesting

that the lower VF preference for hand actions in SPOC and

precuneus is unlikely to be entirely driven by attention.

Nevertheless, the relationship between lower VF preferences

in attention and action deserves further investigation and if

we are indeed measuring attentional biases for objects in

lower VF then it is a unique type of attention associated with

visuomotor processes. As previously suggested, it could be

that humans have better attentional resolution in the lower

VF because the control of most skilled actions unfolds there

(Danckert and Goodale, 2003).

The absence of a lower VF preference in aIPS was some-

what surprising, as this region is strongly involved in grasping

(Binkofski et al., 1998; Murata et al., 2000; Culham et al., 2003,

2006) and has been shown to contain a greater lower field

representation for pointing tasks (Hagler et al., 2007). Note,

however, that this discrepancy could be due to task differ-

ences, as the participants in Hagler et al. (2007) always fixated

centrally and pointing movements were executed towards

different memorized target locations whereas in the current

study the movement biomechanics remained constant while

VF was varied through changes in fixation and the actions

were executed on-line.

Alternatively, the behavioural improvement in grasping

when targets are placed in the lower VF may be related to the

enhanced processing in SPOC rather than the processing in

aIPS. Although SPOC has been more strongly implicated in

arm transport than grip formation based on activation levels

(Cavina-Pratesi et al., 2010), more recently activation patterns

and adaptation suggest that it may also play a role processing

the grip orientation and grip formation in both the human

region (Gallivan et al., 2011; Monaco et al., 2011) and its pu-

tative macaque homologue (Fattori et al., 2009, 2010).

In addition to the regions showing a preference for the

lower VF, we also found that during hand actions (but not

passive viewing) several regions in the right hemisphere (i.e.,

SPOC, aIPS, SPL, cuneus, MOG and SFG) presented a stronger

response to left stimuli relative to right stimuli. Interest-

ingly, no right VF preference was observed in homotopic

regions of the left hemisphere. These observations fit

remarkably well with Perenin and Vighetto’s (1988) classical

study of patients with optic ataxia. In particular, these au-

thors found that while left hemisphere lesions mostly lead

to misreaching deficits using the right hand towards both

hemifields (the so-called hand effect), right-hemisphere le-

sions lead to deficits with both hands in the left VF (the so-

called field effect). Moreover, recent neuroimaging reports

have also observed asymmetries in the activation of left and

right aIPS in movement planning, with similar degrees of

activation in the left aIPS regardless of the hand involved,

but a preference for the left hand in the right aIPS (Jacobs

et al., 2010; Martin et al., 2011). In line with these studies,

all our participants were right-handed and only acted with

their right arm, suggesting that the current results may

reflect the left hemisphere dominance in visuomotor control

(e.g., Gonzalez et al., 2006, 2007). In addition, our findings

also suggest that right-hand actions to objects in the left VF

may require bilateral activation, while right-hand actions to

objects in the right VF mainly depends on left hemisphere

activation. Needless to say that these are mere speculations,

and future experiments should investigate further the left/

right effects reported here by additionally asking partici-

pants to act with their left hand.

5.2. Human versus macaque in action

Our results here lend further support to the proposal that

human SPOC functionally corresponds to the macaque

parieto-occipital complex (areas V6 and V6A; see also Pitzalis

c o r t e x 4 9 ( 2 0 1 3 ) 2 5 2 5e2 5 4 1 2539

et al., 2006;Cavina-Pratesi et al., 2010).AreaV6 isapurelyvisual

area located in the ventral part of the POS characterized by a

retinotopic organization (Galletti et al., 1999a; Luppino et al.,

2005; Fattori et al., 2009). In contrast, area V6A, located

dorsally to V6, is not retinopically organized and contains both

visual andsomaticneurons, aswell asneurons involved inarm

and eye movements (Galletti et al., 1999b; Fattori et al., 2001,

2005, 2009, 2010; Luppino et al., 2005). Recently, Pitzalis et al.

(2006, 2010) were able to map the organization of the possible

human homologue of area V6, lying in the dorsal end of the

POS. In the current study (as well as others from our lab), we

have used the nomenclature of SPOC (superior parieto-occip-

ital sulcus), rather that putative V6 and/or V6A, because (1) to

date there is no generally accepted functional localizer for

human V6A and (2) the hypothesized location of this region in

thehumanbrain is variable among individuals and studies (for

a review see Culham et al., 2008). Moreover, another robust

cluster of activation was found in the left precuneus, in a

location anterior to SPOC, a region also involved in the control

of arm movements in monkeys (e.g., Andersen et al., 1997;

Snyder et al., 1997; Andersen and Buneo, 2002).

Consistent with the present results in human SPOC and the

purported homology, macaque areas V6 and V6A have also

shown to over-represent the lower VF (Galletti et al., 1999a;

Gamberini et al., 2011). Moreover, both SPOC (Quinlan and

Culham, 2007) and V6A (Hadjidimitrakis et al., 2011) over-

represent near (vs far) gaze positions. Taken together, these

results converge to suggest that human SPOC and macaque

V6/V6A over-represent the regions of space where hand ac-

tionsmost frequently occure near space, the lower VF, and, in

right-handers, the right VF (present data and Gallivan et al.,

2009) or in left-handers, both VFs (Gallivan et al., 2011).

5.3. Conclusions

In summary, we showed that SPOC and left precuneus have a

lower VF preference for hand actions in linewith the hypothesis

that these regions play an important role in processing visual

information for the control of arm movements. This indicates

that the neural responses within these regions may reflect the

fact that most of our daily actions occur in the lower VF.

6. Funding

This work was supported by operating grants from the Ca-

nadian Institutes of Health Research (grant number:

MOP84293) and Natural Sciences and Engineering Council of

Canada E. W. R. Steacie Memorial Fellowship to J.C.C. In

addition, S.R. was funded by the Portuguese Foundation of

Science and Technology and Social European Fund (grant

number: SFRH/BPD/65951/2009).

Acknowledgements

We are grateful to Shaun Parekh and Robert Mark for assis-

tance with data collection and to Haitao Yang, Jim Ladich and

Steve Bamford for help with hardware development. We

would also like to thank Fraser W. Smith for commenting on

an earlier version of this manuscript.

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