neural representation during visually guided reaching in...

Neural Representation During Visually Guided Reaching in MacaquePosterior Parietal Cortex

Barbara Heider, Anushree Karnik, Nirmala Ramalingam, and Ralph M. SiegelCenter for Molecular and Behavioral Neuroscience, Rutgers University, Newark, New Jersey

Submitted 1 December 2009; accepted in final form 14 September 2010

Heider B, Karnik A, Ramalingam N, Siegel RM. Neural represen-tation during visually guided reaching in macaque posterior parietalcortex. J Neurophysiol 104: 3494–3509, 2010. First published Sep-tember 15, 2010; doi:10.1152/jn.01050.2009. Visually guided handmovements in primates require an interconnected network of variouscortical areas. Single unit firing rate from area 7a and dorsal prelunate(DP) neurons of macaque posterior parietal cortex (PPC) was re-corded during reaching movements to targets at variable locations andunder different eye position conditions. In the eye position–variedtask, the reach target was always foveated; thus eye position variedwith reach target location. In the retinal-varied task, the monkeyreached to targets at variable retinotopic locations while eye positionwas kept constant in the center. Spatial tuning was examined withrespect to temporal (task epoch) and contextual (task condition)aspects, and response fields were compared. The analysis showeddistinct tuning types. The majority of neurons changed their gain fieldtuning and retinotopic tuning between different phases of the task.Between the onset of visual stimulation and the preparatory phase(before the go signal), about one half the neurons altered their firingrate significantly. Spatial response fields during preparation and ini-tiation epochs were strongly influenced by the task condition (eyeposition varied vs. retinal varied), supporting a strong role of eyeposition during visually guided reaching. DP neurons, classicallyconsidered visual, showed reach related modulation similar to 7aneurons. This study shows that both area 7a and DP are modulatedduring reaching behavior in primates. The various tuning types in bothareas suggest distinct populations recruiting different circuits duringvisually guided reaching.

I N T R O D U C T I O N

Primates rely heavily on the visual guidance of limb move-ments for foraging and social interactions. They have to selecta visual target, move the eyes to the target, and finally followwith the hand to the target (Desmurget and Grafton 2000). Thisreaching process requires transformations between coordinatesystems in time with multiple computational steps involved(Shadmehr and Wise 2005). Areas of the posterior parietalcortex (PPC) play a critical role in the transformation betweenvision and action by combining signals from various corticalareas.

Eye position modulates visual neural responsiveness of PPCneurons (Andersen and Mountcastle 1983; Andersen et al.1985, 1990b; Read and Siegel 1997; Salinas and Sejnowski2001). Reaching studies of the parietal reach region (PRR)suggest that visually guided arm movements are planned ineye-centered coordinates (Batista et al. 1999; Buneo et al.2002; Scherberger et al. 2005; Snyder et al. 2006). In this

study, eye position was either varied together with the reachtarget so that reaching was made to foveated targets, or fixationwas kept constant on the center so that reaching was made tononfoveated targets. The goal of this study was to explore thespecific spatial and temporal relationships between visual,preparatory and reach signals in two regions of the PPC. Area7a and the nearby dorsal prelunate (DP), which is at the mostposterior end of the PPC and believed to be strongly visual,were examined. The DP region has strong feedforward con-nections to area 7a (Andersen et al. 1990a; Cavada and Gold-man-Rakic 1989a), but also receives signals from other pari-etal, frontal, and extrastriate visual areas (Stepniewska et al.2005).

The first hypothesis tested whether eye position and retino-topic tuning of 7a and DP neurons were affected by task phase,especially preparation and initiation of the reaching movement.If different mechanisms or inputs contributed to various signalsin PPC such as eye position and motor planning, we mightexpect differential effects on spatial tuning for the visual,preparatory, and movement initiation phases of the task. Thesecond hypothesis examined the spatial parameters duringpreparation and initiation of the reaching movement betweenthe two task conditions, that is, whether the reach targets werefoveated. Planning and executing a reach movements to targetsin the same body-centered, but different eye-centered coordi-nates, might yield distinct spatial tunings of 7a and DP neuronsbecause both areas are strongly altered by gain fields.

We implemented an “approach” (Gardner et al. 2007), alsocalled “radial” (Fattori et al. 2005) reaching movement, inwhich the hand starts from a position close to the animal’strunk and moves in three dimensions (3D) toward the reachtarget, as used in an area 7a study by MacKay (1992). We usedoptic flow field stimuli as reach targets. This stimulus ensuredthat we activated 7a and DP neurons optimally and allowed tostudy the influence of the reach-related signals modulatingthese visual responses. The delayed reaching task evaluatedvisual stimulus presentation, eye position, preparation, andinitiation of the arm movement activity.

M E T H O D S

Animal preparation

Two male rhesus monkeys (M1R, 11 kg; M3R, 8.5 kg; age �10 yr)were trained on a visually guided reaching task. All proceduresconformed to the National Institutes of Health Guide for the Care andUse of Laboratory Animals; Rutgers University Animal Care andFacilities Committee approved all experimental protocols.

Each animal was prepared for electrophysiological recordings byattaching a head post and recording chamber in separate surgeries. Allsurgeries were performed under sterile conditions with isoflurane

Address for reprint requests and other correspondence: B. Heider, Ctr. forMolecular and Behavioral Neuroscience, Rutgers Univ., 197 University Ave.,Newark, NJ 07102 (E-mail: [email protected]).

J Neurophysiol 104: 3494–3509, 2010.First published September 15, 2010; doi:10.1152/jn.01050.2009.

3494 0022-3077/10 Copyright © 2010 The American Physiological Society www.jn.org

anesthesia. Both monkeys had been previously used for intrinsicoptical imaging of posterior parietal cortex and had imaging chambers(diameter 20 mm) implanted over their right hemisphere (Heider et al.2005; Siegel et al. 2003) contralateral to the left hand used forreaching. This permitted visual identification of areas 7a and DP in thechamber. At the conclusion of the optical imaging studies and beforerecording, the transparent artificial dura was removed, and the naturaldura was allowed to grow back over the brain. If necessary, systemicprophylactic antibiotics were given for this procedure (Ceftriaxone, 50mg/kg). A stainless steel adapter was attached to the optical chamberto hold the stage and microdrive and allow precise, targeted electrodepenetrations into designated areas (Fig. 1).

Experimental setup

During the experiment, the animal’s head was fixed with the headpost attached to a specially designed primate chair that allowed freemovement of the upper limbs. A touch-sensitive panel (Crist Instru-ment, Hagerstown, MD) or capacitive proximity sensor (IFM Efector,Exton, PA) attached to the belly plate of the primate chair ensured thatthe monkey held his reaching hand in a constant launching positionclose to his torso. A touch sensitive monitor (Elo TouchSystems,Menlo Park, CA) positioned 30 or 35 cm (depending on each mon-key’s arm length) from the animal’s eyes recorded the reachingendpoints. Distance from the launching position to the touch screenwas 35–40 cm (depending on the end position of the target). Thereach distance from the start panel to the nine end positions was notvaried in a systematic manner. The experiments were performed in acompletely dark room. However, a faint luminosity of the touchscreen could not be completely eliminated even at the lowest bright-ness settings and completely black background. Thus the monkeycould only perceive his hand when it had reached and partiallyoccluded the reach target.

The NIMH Cortex software (//www.cortex.salk.edu) displayed thestimuli, controlled the behavioral variables, and was synchronized tothe analog spike collection system that was programmed using Matlab(MathWorks, Natick, MA) in conjunction with aPCMCIA-based A/Dconverter (NI DAQCard-6036E, National Instruments, Austin, TX) ina PC-based system.

Stimuli and behavioral task

The fixation dot consisted of a small (0.8° diam) red square. Thevisual reach targets were circular patches of moving dots (12° diam).These were either expansion (76%) or compression (24%) optic flowpatches, which consisted of 128 dots (0.1° diam) with an equivalentangular velocity of 6°/s and a point life of 532 ms. The optic flowpatches were displayed in one of nine positions within a 3 � 3 grid(step 12°, total 36 � 36° area).

The monkeys performed two versions of the reaching task. In theeye position–varied task (EVAR; Fig. 2A), the small fixation dot andthe optic flow reach target were presented together in one of the ninepositions to test the effect of eye position. The optic flow patch waspresented behind the fixation dot, which was visible throughout thetask. Thus the reach target was always foveated ensuring that angle ofgaze and reach position varied jointly, whereas the locus of retinotopicstimulation remained constant over the fovea. In the retinal-varied

A1 2 3 4

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FIG. 2. Display for (A) the eye position–varied (EVAR) and (B) retinal-varied tasks (RVAR) and (C) task sequence. Numbers in each panel indicateepochs of interest. 1) Baseline fixation period with hand on the launch panel(1,500 ms). The fixation dot appears immediately after the animal places hishand on the launch panel. 2) Visual stimulation period (optic flow reach target)during which the hand remains on the launch panel (2,000–3,000 ms). Thestimulus appears at the top right location (coordinates 12,12°) in the schematic(A and B). 3) Stimulus change (structured to unstructured motion of optic flow)instructs the monkey to lift his hand off the panel. 4) Reach period after thehand is lifted off the panel. Throughout the task, the monkey has to maintainfixation on the fixation dot. Epochs for analysis of neural activity are indicatedby gray-shaded rectangles.

FIG. 1. Recording sites in optical chamber (M1R). Image of blood vesselpattern (green light, 540 nm) and grid with recording sites overlaid on chamberpicture with regrown dura. Area 7a is located between intraparietal sulcus(IPS) and superior temporal sulcus (STS; filled circles mark recording sites);the dorsal prelunate (DP) is located between lunate sulcus (LS) and STS (opencircles mark recording sites). Grid, 1-mm spacing. Small inset shows anatom-ical overview of the right hemisphere of M1R reconstructed from structuralMRIss. White circle marks location of recording chamber relative to the sulcalpattern.

3495PROPERTIES OF PARIETAL NEURONS FOR REACHING

J Neurophysiol • VOL 104 • DECEMBER 2010 • www.jn.org

task (RVAR; Fig. 2B), the fixation dot always appeared in the centerof the screen (primary position 0, 0°), and the optic flow target wasdisplayed in one of the nine positions. Thus the reach target was notfoveated, except for the center target, and retinotopic stimulation wasvaried. In both tasks, the monkeys were required to touch the targetswithin the 12°-target diameter.

The temporal sequence of task events was always as follows (Fig.2C). A trial started only when the left hand rested on the touch-sensitive launching panel. Then, the fixation dot appeared and themonkey started fixating within 500 ms. After 1,500 ms, the optic flowtarget was displayed. Randomized between 2,000 and 3,000 ms afterstimulus onset, the structured optic flow changed to unstructuredmotion; thus the duration of the delay period was variable. Within a600-ms reaction time, the animal made a hand movement to the target.Once the hand landed on the touch screen, the monkey had to hold hishand on the optic flow target for 1,500 ms. The target remained inplace during this period. A drop of juice rewarded the animal forsuccessful completion of the trial.

If the monkey did not acquire fixation within the 500-ms time, thetrial was aborted, and a new trial started after 500 ms. Launching thehand incorrectly, that is, too early before or too late after the stimuluschanged, terminated the trial immediately. The monkey performed aminimum of 10 trials per condition (total of 90 correct responses foreither RVAR or EVAR task). The two tasks were performed inseparate blocks of trials with their order varied.

An infrared eye camera (ISCAN, Cambridge, MA) in conjunctionwith the NIMH Cortex system monitored and collected eye positionnoninvasively at 60 Hz. The eye movement window was kept at 4° tocontrol fixation; this value conforms to other reaching studies (Batistaand Andersen 2001; Battaglia-Mayer et al. 2001, 2005; Marzocchi et

al. 2008; Scherberger et al. 2003; Snyder et al. 2006). If the monkeyfixated outside this window, the trial aborted immediately.

The eye movements were examined off-line at two time points(stimulus onset and lift hand) in the two tasks. One experiment showstypical eye movement traces for two task conditions (Fig. 3). Theaverage eye position traces (10 trials) at the lift hand event for the ninereaching locations are plotted. Although fixation was not as precise asin pure fixation tasks (Andersen et al. 1985, 1990a; Goldberg et al.2002; Siegel and Read 1997), we could find no bias with differentstimulus presentations, hence the larger 4° fixation window. In theEVAR task, no eye movements were associated with the differentfixation positions at the lift hand event (Fig. 3A). Most importantly, inthe RVAR task, there was no biased eye movement toward the opticflow target at the time of hand lift (Fig. 3B). The average horizontaland vertical eye position from each experiment were transformed intovectors to quantify these effects (Fig. 3, C and D). The difference invector amplitude 500 ms before and after lift hand was computed. Inthe example shown, eye position shifts averaged 1° for the EVAR taskand 0.8° for the RVAR task. In comparison, eye position shifts at theonset of the optic flow stimulus were on average 2.2° in the EVARand 1.5° in the RVAR task. These findings were similar acrossexperiments. Thus changes in eye position at the time of the reachevent were minimal and could not be responsible for differences inneural activity between tasks.

Neural recordings

Neural responses were recorded extracellularly with platinum-iridium electrodes (UEPSEGSG2N5G, FHC, Bowdoinham, ME) withan impedance of 0.5–2.5 M�. Penetrations were oriented orthogonal

FIG. 3. Eye movements before and afterreach movement for both EVAR and RVARtasks in 1 experiment (MFR260.C01). A andB: horizontal (gray) and vertical (black) eyeposition traces aligned to the reach event(“lift hand event,” dashed line) showing 1.5s before and after. The 9 panels (3 � 3) forEVAR (A) and RVAR (B) tasks represent 1typical experimental trial for each position(position in degree visual angle indicatedwithin each panel). C and D: mean deviation(eye position 500 ms before event subtractedfrom 500 ms after event) averaged over 10repetitions per position for EVAR (C) andRVAR (D) tasks.

3496 B. HEIDER, A. KARNIK, N. RAMALINGAM, AND R. M. SIEGEL


to the cortical surface. The electrode was advanced using a hydraulicmotor drive (David Kopf Instruments, Tujunga, CA). After passingthrough the dura, the depth of the first occurrence of neural activitywas recorded, and recordings were confined to 2,000 �m from the topof neural activity. We also recorded activity when retracting theelectrode to confirm depth measurements in case of dimpling. Aver-age depth of all recordings was 1,140 � 565 (SD) �m (n � 155). Perpenetration, about one to five units were recorded. Because the sulcalpattern of the PPC was visible through the transparent artificial dura,the two cortical regions of interest could be located without killing theanimal (Fig. 1). Area 7a was operationally defined as the cortexbetween the intraparietal sulcus (IPS) and the end of the superiortemporal sulcus (STS) in agreement with earlier studies (Heider et al.2005; Siegel et al. 2003). DP was defined as the region between theSTS and the lunate sulcus (LS).

Neural activity was amplified (Model 1800 Microelectrode AC Am-plifier, A-M Systems, Carlsborg, WA), fed through a Humbug 50/60 Hznoise eliminator (AutoMate Scientific, Berkeley, CA), band-pass filtered(300–20,000 Hz), digitized at 40 KHz, and spikes separated off-line withspike sorting software (Off-line Sorter 1.39, Plexon, Dallas, TX). Allsubsequent quantitative analyses were done on the off-line sorted data.Units were isolated on-line with a dual-window discriminator (BAK,Germantown, MD) to assess neural selectivity during recording.

To obtain a sample as unbiased as possible, activity from allneurons that could be sufficiently isolated were recorded regardless ofwhether a neuron displayed a preference for the visual or reach aspectof the task. In about one half of all units recorded, preference for typeof motion (expansion, compression, and 2 rotational flows) was testedwith a centrally presented large field optic flow patch (20° diam).Most area 7a or DP neurons responded robustly to either expansion orcompression optic flows as reported previously (Merchant et al. 2001;Read and Siegel 1997; Siegel and Read 1997); thus these two types ofstimulus were used for the majority of units. In instances where visualpreference for type of optic flow could not clearly be established fromthe on-line neural response, expansion flow was used.

Spike analyses

Analog data were analyzed off-line with the Plexon software, andspikes were identified by comparing waveforms over the course of theexperiment in conjunction with Khoros (Khoral Research, Albuquerque,NM) and custom UNIX-based software. Spike rasters were synchronizedto different task events (Fig. 2C, dashed lines), and the firing rate for theepochs of interest was calculated (Anderson and Siegel 1999; Siegel andRead 1997): 1) baseline activity during fixation before stimulus onset; 2)after stimulus onset to determine visual responsiveness (visual epoch); 3)before cue to lift (i.e., stimulus change) to determine movement prepa-ration activity before the reach movement (preparatory epoch); and 4)after lift hand from starting panel to determine reach initiation activity(reach epoch). For the baseline, visual, and preparatory epochs, 500-msintervals were used. For the reach epoch, a 300-ms interval was used toavoid contamination from the tactile or visual cues when the handtouched the screen.

Categorical regressions

To directly quantify the spatial relationship between the differentepochs on a neuron-by-neuron basis, a multiple step procedure wasfollowed. The individual firing rates for all four epochs was first com-puted. To simultaneously examine the dependency of firing rate on typeof epoch and reach target position, a stepwise categorical quadraticregression model was applied. The model for the firing rate was

A(x, y, E, i) � ax[E]x � ay[E]y � axy[E]xy� axx[E]x2 � ayy[E]y2 � b[E] � �i

A(x,y,E,i) is the firing rate for the ith trial. E is the epoch underconsideration, which has four categorical values, corresponding to the

baseline, visual, preparation, and reach epochs. x and y are thepositions of the target on the screen in degrees of visual arc. ax[E]xrefers to the four categorical coefficients for the linear dependence onthe horizontal position. axx[E]x2 refers to the four possible categoricalcoefficients for the second-order dependence on the horizontal posi-tion. Similar terms are found for the vertical ay[E]y and ayy[E]y2

coefficients and the interaction term axy[E]xy. b[E] is the intercept thatcan differ for the four categorical epochs. �i is the error for the ith trial.The coefficients (e.g., ax[E]x) were selected using a stepwise algo-rithm that determined whether the quartet of coefficients wassignificantly different from zero. At the conclusion of the stepwisealgorithm, only coefficients remained that were statistically signif-icant from zero at P � 0.05. The categorical regression wasimplemented using procedures GLMOD and REG (SAS Institute,Cary, NC). This analysis thus concluded with values that weresignificant at P � 0.05.

TIME-DEPENDENT TUNING. The combination of significant regres-sion parameters determined the tuning type for each neuron. Neuronswith uniform firing rates across target positions (P) but different meanfiring rates across epochs (E) were termed type E. Neurons withsignificantly different spatial parameters (ax, ay, axy, axx, ayy) acrossepochs have multiplicative interactions between position and epochand were termed multiplicative type E�P. These cell response fieldschanged shape between epochs, that is, their eye position (EVARtask) or retinotopic (RVAR task) spatial tuning was altered as the taskprogressed. Finally, there were nonsignificant cells with neither epochnor position effects (NS). Two other tuning types could potentiallyresult from the categorical regression analysis but were not encoun-tered: 1) cells that had at least one significant spatial parameter andmaintained the same firing rate between epochs (type P) and 2) cellswith at least one significant spatial parameter, which remained con-stant across epochs, and significant changes in overall firing ratebetween epochs (E�P).

TASK-DEPENDENT TUNING. To examine the effects of task on neuralreaching activity, categorical regressions examined the effect of task(T, RVAR vs. EVAR) and position (P) separately during the prepa-ratory and reach epochs, because they represent crucial stages of thereaching task. This analysis again showed three different interactiontypes. Neurons with uniform firing rates across positions but differentmean firing rates between tasks were called type T. Neurons thatchanged spatial parameters between tasks (multiplicative type T�P)had response fields that differed significantly between tasks. Nonsig-nificant cells (type NS) that had neither task nor position effects werealso found. Again, there were no pure position cells (type P) nor werethere any additive cells (type T�P).

Both the time-dependent and the task-dependent population spatialparameters were computed for the multiplicative types. For cells withsignificant linear horizontal and vertical coefficients (ax, ay), thedirection of spatial tuning was summarized by the x- and y-vectors.The population spatial parameters were assessed with circular statis-tics. First, the resulting vectors were transformed into polar coordi-nates, that is, � � arctan (ay/ax) with the convention of 0° (360°)corresponding to the right position “East” (12, 0°) with a counter-clockwise rotation. For the population of vectors, the Hotellingone-sample test (Batschelet 1981; Zar 1984) determined whethervectors were distributed nonuniformly. This statistic uses the ampli-tude and the direction of the angular tuning. Therefore a weaklyspatially tuned cell (i.e., with small linear coefficients) contributes lessto the statistic than a strongly tuned cell for a given direction.Significance level for the resulting F-test was set at P � 0.05. Toexamine changes in spatial tuning, the directions of the differencevectors (axprep � axvis, ayprep � ayvis) were computed between thepreparatory and visual epoch. Such a comparison shows modulationearly and late in the delay period and thus reflects increasing influ-ences from nonvisual signals.



In cells with mixed linear and quadratic coefficients, the dimensionsof the resulting response fields were determined based on the combi-nation of significant parameters (ax, ay, axx, ayy), similar to previousstudies (Heider et al. 2005; Quraishi et al. 2007). Cells that had aquadratic dependence along both the horizontal and vertical had alocal maximum (“peak,” negative axx and ayy terms), a local mini-mum (“trough,” positive axx and ayy terms), or a “saddle” shapedresponse field (different signs for axx and ayy terms). For the two lattercombinations, the highest firing rate is located in the periphery ofvisual space. Thus for cells with quadratic coefficients, the preferreddirection (maximum response) can only be established for cells withnegative quadratic coefficients (peaks) and without interaction param-eters (axy). To visualize the spatial tuning for each significant cell,response fields derived from the quadratic, and linear coefficientswere created.

To determine whether neural responses differed between two ep-ochs (visual vs. preparatory) on a trial-by-trial basis, the firing ratewas computed for the two epochs averaged across all nine positions.The averaged firing rate was compared with a paired t-test generatinga probability value, P. The number of neurons with a probability ofP � 0.05 was calculated. This analysis is called paired analysisthroughout the paper. For comparison of cell type distributions, a �2

test was used with a significance level of P � 0.05.

R E S U L T S

Behavioral data

Behavioral measurements consisted of reach endpoint accu-racy relative to the center of the target and response times.

Endpoints on the screen from one experiment (EVAR andRVAR) are plotted in Fig. 4. This example shows that reachingwas more accurate (i.e., closer to the target center) in theEVAR than RVAR task. A paired comparison of the vectorsderived from the horizontal and vertical endpoint positionsconfirmed that accuracy was indeed greater in the EVAR taskwhen the reach target was foveated (t-test, P � 0.007). Thelower endpoint accuracy in the RVAR task may be the result ofthe larger difference between reach endpoint and fovea and theknown gaze-dependent errors when pointing to peripheraltargets (Henriques and Crawford 2000).

Two behavioral time segments were computed for all exper-iments: reaction time (RT), that is, the period from the changein optic flow to the hand lift, and movement time (MT) fromthe hand lift to the moment the hand touched the screen. Thesetwo time segments were compared between the RVAR andEVAR task for 98 recordings where both tasks were completed(Fig. 5). Within an experimental recording, MTs from startpanel to touch screen were significantly shorter in the RVARtask (t-test, P � 0.001) than in the EVAR task (Fig. 5A).

For the RTs (Fig. 5B), there were no significant differencesbetween the EVAR and the RVAR tasks with respect to themean. The pairwise plots examined how these behavioralparameters varied on a day-by-day basis. Both movementtimes and reaction times varied between experiments but weresignificantly correlated between tasks within a day (Fig. 5, A

Y-position(deg)

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FIG. 4. Reach endpoints of 1 typical experiment (n � 90trials, MFR256.C01) during the EVAR task (A, Œ) and theRVAR task (B, �). Dashed circles indicate circumference ofoptic flow patches (diameter 12°).

FIG. 5. Distribution and scatter plots ofmean behavioral times (T) for the 2 tasks(TEVAR: EVAR; TRVAR: RVAR). �, behav-ioral times that were significantly different(TEVAR vs. TRVAR) with Student’s t-test; Œ,nonsignificant values. Along each axis, his-tograms show distribution of behavioraltimes for the significant (filled bars) andnonsignificant (open bars) values. The an-gled histograms represent TEVAR � TRVAR.A: movement times (time from hand lift totouch). B: reaction times (time from stimuluschange to hand lift). Each dot represents themean of the behavioral times during 1 re-cording run (90 trials).



and B). Some days, the monkey responded very fast, whereason other days, reaction and movement times were slower inboth tasks. The two animals differed in their mean detectionand travel times but showed the same task effects.

Across all experiments, the average reach velocity was �1.2m/s, which lies well within published data for fast, ballisticreaching (Churchland et al. 2006; Gardner et al. 2007; Kurataand Hoshi 2002). These behavioral reach data were obtainedlargely without visual feedback (Desmurget and Grafton 2000;Vercher et al. 1994), because the monkey could not see hishand until it reached the touch screen. The slower speed (i.e.,longer movements times) found when reaching to foveatedtargets in the EVAR task matches published studies in humans(Prablanc et al. 1986). These behavioral differences betweenthe two task conditions suggest different computational strat-egies and have to be considered when interpreting the singleunit data (Moran and Schwartz 1999; Snyder et al. 2006).

Electrophysiological dataset

The main goal of this study was to examine the spatialrelationship between baseline, visual, preparatory, and reachsignals in area 7a and DP. The statistical analyses thus focusedon temporal (epochs), spatial (reach target position), and con-textual (task condition) aspects of the neural response. A totalof 164 units (90 in M1R, 74 in M3R; 99 in area 7a, 65 in DP)were studied quantitatively using the EVAR task. For theRVAR task, 119 units were studied (62 in M1R, 57 in M3R; 65in area 7a, 54 in DP). For a total of 98 cells, both the RVARand EVAR tasks were completed (53 in 7a; 45 in DP).

The data are presented three ways. First, the epoch-basedanalysis and modeled response fields are exemplified for onearea 7a and one DP cell. Second, the epoch-based analysisexamines temporal and spatial aspects within the EVAR andRVAR tasks for the population of neurons. Third, the EVARand RVAR tasks are compared directly during preparatory andreach epochs to show the effect of eye position.

Single unit activity synchronized to task epochs

EVAR TASK. The 7a neuron (Fig. 6, A–D) responded stronglyduring all epochs in the EVAR task. The baseline activitybefore stimulus onset was strongest for the contralateral (left)eye positions (Fig. 6A, light gray–shaded bars). The neuronresponded with a transient burst of activity to the onset of thevisual stimulus for the contralateral and lower eye positions(Fig. 6A, dark gray–shaded bars). The baseline and visualactivity resulted in two differently shaped response fields (Fig.6B). During the preparatory epoch, the spatial preferenceremained constant, with higher activity for the contralateraland lower eye positions (Fig. 6, C and D). After the lift handevent, the spatial preference shifted upward toward the midline(Fig. 6, C and D).

The DP neuron (Fig. 6, E–H) had a weak spatial tuningduring the baseline fixation epoch with elevated activity for thelower ipsilateral (right) eye positions (Fig. 6E). Steep increasesin activity were observed at stimulus onset for the contralateraland ipsilateral eye positions (Fig. 6E), resulting in a saddleshaped response field (Fig. 6F). This eye position tuningchanged during the preparatory epoch (Fig. 6G) with a prefer-ence for lower contralateral targets. During the reach epoch,

firing increased further for the lower center position (Fig. 6G)and changed the shape of the response field (Fig. 6H).

The spatial tuning across time for both neurons is shown byplotting the linear coefficients (Fig. 7). The 7a neuron (Fig. 7A)started with an upper contralateral eye position tuning duringbaseline (B) and shifted to a lower contralateral tuning whenthe stimulus appeared (V). During the preparatory epoch, thistuning moved toward the vertical midline (P) and finallyupward toward the center after the monkey launched thereaching movement (R). The DP neuron (Fig. 7B) shifted eyeposition tuning from lower ipsilateral (B) to contralateral (V,P) and back to the lower ipsilateral eye positions (R) as the taskprogressed.

RVAR TASK. The 7a neuron exhibited a distinct retinotopictuning when fixation was kept constant on the center position(Fig. 8, A–D). Baseline tuning was flat (Fig. 8, A and B) asexpected. At stimulus onset, the neuron fired for targets ap-pearing in the lower contralateral visual field (Fig. 8A), result-ing in a tilted response field (Fig. 8B). During the preparatoryepoch, the retinotopic tuning remained in the lower contralat-eral visual field (Fig. 8, C and D) and then moved furtherupward toward the midline (Fig. 8, C and D) during the reachepoch.

The DP neuron’s response field was flat during the baselineperiod (Fig. 8, E and F). Stimuli appearing in the center andipsilateral visual field yielded increased neural activity (Fig.8E), resulting in a peaked response field for the visual epoch(Fig. 8F). The preparatory epoch was characterized by stronglyelevated activity for the upper ipsilateral retinotopic targetsyielding a steeply tilted response field (Fig. 8, G and H). Afterthe lift hand event, the firing rate sharply decreased, especiallyfor those positions that showed peak firing during the prepa-ratory epoch (Fig. 8G). During the reach epoch, the highestfiring rates were seen for the lower ipsilateral targets (Fig. 8, Gand H).

The corresponding plot of the linear coefficients for the 7aneuron during the RVAR task (Fig. 9A) shows how the cell’sspatial preference started in the center during baseline (B) andmoved toward the lower contralateral visual field after stimulusonset (V). During preparation (P) and initiation of the reach(R), the retinotopic spatial tuning shifted back toward thecenter. The DP neuron (Fig. 9B) switched its retinotopic spatialtuning from center (B) toward the ipsilateral visual field atstimulus onset (V), further ipsilateral during preparation (P),and downward during reach (R).

Comparison of spatial tuning between epochs

These two example neurons show the complex interactionsbetween reach target location and epoch. Area 7a and DPneurons altered their spatial eye position and retinotopic tuningduring the task. To quantify such changes for the population ofrecorded neurons, different tuning types were determined usingthe results of the categorical regression. Cells were classified as1) having significant changes in overall firing rate withoutspatial tuning (type E), 2) having time-variant spatial tuning(type E�P), or 3) cells without effects (type NS).

EVAR TASK. The majority of cells (70%, 114/164) showed aneffect of epoch and/or position as quantified by the statisticalcategorical regression (Fig. 10A). The distribution of the two



tuning types (E, E�P) did not differ significantly betweenareas. Area 7a and DP also contained neurons that did notrespond during any of the selected epochs (NS, total: 30%,50/164; 7a: 35%, 35/99; DP: 23%, 15/65). The type E neuronsshowed flat spatial tuning and significant differences in inter-cepts between at least two epochs (total: 10%, 17/164; 7a:

12%, 12/99; DP: 8%, 5/65). Comparison of intercepts betweenvisual and preparatory epochs did not show significantdifferences.

The multiplicative (type E�P) neurons comprised 59% ofthe cells (total: 97/164; 7a: 52%, 52/99, DP: 69%, 45/65).These cells were fit with at least one significant spatial param-

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FIG. 6. EVAR task. A–D: area 7a neuron(MFR270.C01, expansion optic flow). A: spikerasters and peristimulus time histograms(PSTHs) for the 9 reach targets aligned tostimulus onset event (baseline and visual ep-ochs, light-shaded and dark-shaded regions,respectively). Each subpanel of the 3 � 3panels represents neural responses for 1 targetlocation. Bin width, 50 ms. B: quantitativemodeled response fields for baseline (B) andvisual epochs (V). Equations are for firing ratein hertz. Abase � �0.71x � 0.21y � 0.021x2 �0.078y2 � 27.4. Avis � �0.46x � 0.76y �0.115x2 � 0.074y2 � 30.5. C: spike rastersand PSTHs aligned to reach cue event (prepa-ratory epoch, dark-shaded region, left half ofeach subpanel) and lift hand event (reach ep-och, dark-shaded region, right half of eachsubpanel). D: response fields for preparatory(P) and reach (R) epochs. Aprep � �0.26x �0.61y � 0.036x2 � 0.023y2 � 24.2. Areach ��0.12x � 0.094y � 0.132x2 � 0.019y2 �40.8. E–H: area DP neuron (MJR085.C01,expansion optic flow). E: rasters and PSTHsaligned to stimulus onset. F: response fields.Abase � 0.17x � 0.37y � 0.02x2 � 0.001y2 �11.5. Avis � �0.12x � 0.39y � 0.051x2 �0.05y2 � 20.1. G: rasters and PSTHs alignedto reach cue and lift hand. H: response fields.Aprep � �0.44x � 0.58y � 0.023x2 � 0.03y2 �14.5. Areach � 0.31x � 0.37y � 0.042x2 �0.037y2 � 14.8.



eter (ax, ay, axy, axx, ayy) during at least two of the four epochs.Of these 97 E�P cells, 85 had at least two significant spatialparameters for the visual, preparatory, and/or reach epochs.Forty-one of the 97 E�P cells (42%) were only linearlymodulated by the stimulus position. In these cases, the hori-zontal (ax) and vertical (ay) terms indicate the maximumresponse for the preferred eye position. For all epochs, theangular eye position tuning was distributed uniformly for thispopulation of E�P neurons. A uniform distribution was alsopresent for the vector of the spatial shifts between visual andpreparatory epochs. Another 36% (35/97) of E�P neurons hadan additional quadratic dependence in at least one dimension.Significant interaction terms were present in 21% (20/97) ofthe E�P neurons.

The differences in firing rate between visual and preparatoryepochs were established using the paired analysis (see METH-ODS), which computed the change in activity between prepara-tory and visual epoch for each E�P neuron. For this group,43% of neurons (7a: 22/97; DP: 20/97) had significantlydifferent firing rates. During these two epochs, the monkey wasmaintaining fixation at one location, the visual stimulus re-mained constant (i.e., structured optic flow), and the hand wasresting on the start panel. Thus changes in neural activity canbe attributed only to internal processing (e.g., motor planning,attention).

RVAR TASK. With the eye position kept constant at the primaryposition (0, 0°), about two thirds (63%, 75/119) of the cells hadan effect of epoch and/or position (Fig. 10B). The distributionof the two tuning types (E, E�P) was similar between areas.Area 7a and DP also contained neurons that did not respondduring any of the selected epochs (NS, total: 37%, 44/119; 7a:38%, 25/65; DP: 35%, 19/54). The type E neurons weremodulated by the event but had no spatial retinotopic tuning(total: 18%, 21/119; 7a: 17% 11/65; DP: 19% 10/54). Inter-cepts for the visual epoch were significantly higher than for thepreparatory epoch (t-test, P � 0.006), suggesting that havingretinotopically varied stimuli yielded high firing rates imme-diately after stimulus onset, which decreased substantiallytoward cue event. These type E cell receptive fields could belarge and bilateral as reported previously (Motter and Mount-castle 1981; Mountcastle et al. 1987), therefore not showingsignificant spatial modulation from the limited display size(36 � 36°).

The multiplicative (type E�P) neurons comprised 45%(total: 54/119; 7a: 45%, 29/65; DP: 46%, 25/54) of the cells.Pure linear modulation was present in 30% (16/54), whereas33% (18/54) of E�P neurons had an additional quadraticdependence. For population of purely linear cells, angulartuning was uniformly distributed. Significant interaction termswere present in 22% (12/54) of the E�P neurons. Among the54 E�P cells, 43 had significant spatial parameters for thevisual, preparatory, and/or reach epoch. With the paired anal-ysis, it was found that 52% of the E�P neurons (7a: 14/54; DP:14/54) significantly changed their firing between the visual andpreparatory epoch.

In summary, the regression analysis provided a robust quan-titative measure of the differential effects of epoch on aneuron-by-neuron basis during the EVAR and RVAR tasks.About two thirds of the cells were altered by epoch as the taskprogressed, more often in form of changes in spatial tuningthan in form of gain changes. Although the stimulus on thescreen provided constant visual stimulation throughout thetask, additional spatially tuned inputs related to the preparatoryand reach event impacted these neurons’ activity.

Comparison of single unit activity between RVARand EVAR task

Neural activity during the preparatory and reach epochs wasdirectly compared on a neuron-by-neuron basis for conditionswhere the location of the reach targets was identical, but reachmovements were made under different combinations of eyeand retinal information. In the EVAR task, the monkey reachedto a foveated target; thus eye position varied concurrently withreach target position, whereas the retinotopic stimulation re-mained constant on the fovea. In the RVAR task, the target wasnot foveated (except for the center position) and the retinotopicstimulation varied. A subset of 98 cells was analyzed in whichboth the EVAR and RVAR tasks were tested. Categoricalregressions determined the effects between the two factors:task condition (T, EVAR vs. RVAR) and position (P, 9reach target positions). These effects were determined sep-arately for each of the four epochs, but the focus will be onthe preparatory and reach epochs. Neurons were groupedaccording to whether they changed their tuning in the task orspatial domain.

FIG. 7. Changes in spatial eye position tuning (EVAR) forthe example area 7a (A) and DP (B) neurons (see Fig. 6). Blackarrows indicate shifts in spatial preference (linear coefficients)between baseline, visual, preparatory, and reach epochs.



BASELINE AND VISUAL EPOCHS. Firing rate for the center posi-tion was compared between EVAR and RVAR tasks to identifypossible contributions from attentional or other effects betweenthe two task blocks. For both epochs, firing rates did not differsignificantly between the two tasks.

PREPARATORY EPOCH. This epoch is characterized by an ab-sence of sensory or motor changes. The monkey is fixating, astructured optic flow stimulus is displayed, and the hand isresting on the launching panel. During this epoch, the taskfactor affected 76% (74/98) of the cells significantly (Fig. 11A),

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FIG. 8. RVAR task. A–D: area 7a neuron(MFR270.C01); conventions as in Fig. 6.A: spike rasters and PSTHs aligned to stimulusonset. B: response fields. Abase � �0.061x �0.18y � 0.079x2 � 0.025y2 � 38.6.4. Avis ��2.27x � 1.4y � 0.026x2 � 0.007y2 � 38.6.C: spike rasters and PSTHs aligned to reach cueand lift hand. D: response fields. Aprep ��1.46x � 1.05y � 0.01x2 � 0.082y2 � 38.6.Areach � �1.29x � 0.56y � 0.057x2 � 0.12y2 �38.6. E–H: area DP neuron (MJR085.C01).E: rasters and PSTHs aligned to stimulus on-set. F: response fields. Abase � 0.077x � 0.09y �0.024x2 � 0.018y2 � 11.4. Avis � 0.39x �0.19y � 0.011x2 � 0.113y2 � 23.8. G: rastersand PSTHs aligned to reach cue and lift hand.H: response fields. Aprep � 0.64x � 0.1y �0.006x2 � 0.021y2 � 19. Areach � 0.26x �0.65y � 0.06x2 � 0.013y2 � 21.3.



suggesting that the majority of cells changed their tuning orgain depending on whether the hand was going to be moved toa foveated or peripheral reach target. The two tuning types (T,T�P) were distributed evenly between area 7a and DP. Aboutone quarter of the neurons were not affected by either factor(NS, total: 24%, 24/98; 7a: 30%, 16/53; DP: 18%, 8/45). Thetype T was observed in 30% of the cells (29/98; 7a: 30%,16/53; DP: 29%, 13/45). These cells differed in their meanfiring rates between RVAR and EVAR conditions but had flatspatial tuning. Intercepts did not differ significantly betweenthe two conditions for this group.

The multiplicative type T�P was present in 46% of cells(total: 45/98; 7a: 40%, 21/53; DP: 53%, 24/45). In this groupof neurons, identical reach targets yielded different spatialtuning during the preparation of the reaching movement. Typ-ical response fields of 7a cells are shown in Fig. 12A. This cellshowed peak firing for upper ipsilateral retinotopic targets(positive vertical and horizontal coefficients) during the RVARtask. When reaching was performed to foveated targets(EVAR), spatial preference shifted toward eye positions alongvertical midline (Fig. 12E, gray arrow). Another DP cellexample fired mostly for targets in the contralateral hemispaceduring RVAR condition and moved its preference toward theupper contralateral space during EVAR condition (Fig. 12, Band F, gray arrow).

Similar to the analysis of the E�P cells, the T�P cellsduring the preparatory epoch were fit with at least one signif-icant spatial parameter (ax, ai, axy, axx, ayy) during both tasks.Sixteen of these 45 cells (36%) were only linearly modulated

by the target position. Angular tuning distribution for thesepurely linear T�P cells was uniform. Directions of spatialshifts between linear parameters for the EVAR and RVARconditions were also uniform. Another 40% of T�P neurons(18/45) had an additional quadratic dependence in at least onedimension. Significant interaction terms were present in 27%(12/45).

REACH EPOCH. This epoch differed from the preparatory epochby the additional sensory and motor changes (visual stimuluschange and the onset of hand movement initiation). The ma-jority of the cells (total: 81%, 79/98; 7a: 79%, 42/53; DP: 82%,37/45) showed significant task effects (Fig. 11B), confirmingthe hypothesis that the activity during movement initiation wasstrongly affected by the task condition, that is, whether themonkey was going to reach to a foveally or eccentricallypresented stimulus. There were no significant differences indistribution of the T and T�P types between the two areas.Nonsignificant cells comprised 19% of the population (NS,total: 19/98; 7a: 21%, 11/53; DP: 18%, 8/45). About onequarter of the cells were type T neurons (total: 27% 26/98; 7a:28%, 15/53; DP: 24%, 11/45). Intercepts between RVAR andEVAR conditions for this group did not differ significantly.

More than one half of the cells were of the multiplicativetype T�P (total: 54%, 53/98; 7a: 51%, 27/53; DP: 58%,26/45). Thus identical reach target positions yielded varyingspatial preferences depending on whether the target was fove-ated or not. The area 7a cell changed spatial preference fromupper to lower contralateral reach positions between EVAR

FIG. 9. Changes in spatial retinotopic tuning (RVAR) forthe example area 7a (A) and DP (B) neurons (see Fig. 8).Conventions as in Fig. 7.

FIG. 10. Proportions of interaction typebetween epoch (E) and position (P) plottedseparately for each area (7a, filled bars; DP,open bars) during EVAR (A) and RVAR (B)task conditions. E-type neurons had a singleeffect of epoch (change in mean firing rate)but were not spatially tuned. E�P-type neu-rons (multiplicative interaction) had differ-ent spatial tuning between epochs. NS cellshad no effect of either factor.



and RVAR task (Fig. 12, C and E, black arrow). The DP cellshifted preference from upper to lower reach positions betweenRVAR and EVAR tasks (Fig. 12, D and F, black arrow).Seventeen of these 53 cells (32%) were only linearly modu-lated by the target position and had a uniform distribution ofspatial tuning. Spatial shifts between EVAR and RVAR con-ditions were also distributed uniformly. Another 38% of theT�P neurons (20/53) had an additional quadratic dependencein at least one axis. Significant interaction terms were presentin 28% (15/53) of the T�P neurons.

D I S C U S S I O N

Combined findings from various studies have lead to thegeneral consensus that PPC neurons are involved in goal-directed behaviors including attentional and motor planningsignals (Andersen et al. 1997; Burnod et al. 1999; Coulthard etal. 2008; Rozzi et al. 2008; Snyder et al. 2006). This studybuilds on prior reaching studies in area 7a (Battaglia-Mayer etal. 2005, 2007; Blum 1985; MacKay 1992; Mountcastle et al.1975; Rushworth et al. 1997) and expands our knowledgeabout PPC neurons, including DP. First, spatial tuning wasquantitatively compared between the baseline, visual, prepara-tion, and initiation phases of the reaching task. Modeledresponse fields show the changes in spatial tuning over time.Second, area 7a and DP neurons were classified into subpopu-lations with distinct spatial and temporal tuning properties.Third, the role of eye position on reaching activity was exam-ined by having the monkeys reach to foveated (EVAR task) ornonfoveated (RVAR task) targets. Fourth, and importantly, DPwas identified as containing neurons that are modulated duringthe planning and initiation phases of the reaching task.

Methodological considerations

In this study, reaching movements occurred in a radial (3D)manner. This differs from a lateral reach, where the monkeystarts the reach from a target on the screen and then lifts thehand briefly off the screen to move to the next target on aplane, as used in many reaching studies (Batista and Andersen2001; Battaglia-Mayer et al. 2005, 2007; Scherberger andAndersen 2007; Snyder et al. 2006). A radial reach moreclosely resembles a natural movement (MacKay 1992). Be-cause the animal was fixating before making the reach move-ment, the hand could not be seen until it hit the screen andpartially occluded the optic flow target.

Neural responses during different epochs

About one half of the neurons responded to the onset of thevisual stimulus and showed effects of eye and retinal position,as demonstrated previously (Battaglia-Mayer et al. 2007; Fi-scher and Boch 1981a,b; Maguire and Baizer 1984; Merchantet al. 2001; Mountcastle et al. 1987; Read and Siegel 1997;Siegel and Read 1997; Youakim et al. 2001). Within each taskcondition (EVAR or RVAR), we assume that the initial visu-ally dominated response was affected by multiple signalsduring the preparatory and reach epochs.

PREPARATORY RESPONSES. The preparatory epoch was opera-tionally defined as the 500 ms before the cue to reach. Changesin neural firing during this delay epoch were not contaminatedby overt sensory events or motor behaviors. The visual stim-ulus was a constant optic flow, and the hand remained at aresting position. As the target appeared on the screen severalseconds before the cue to reach, the monkey had enough timeto shift his attention and anticipate the upcoming reach cue. Itis very likely that the preparation of the reaching movementbegan as soon as the fixation spot and/or reaching targetappeared on the screen. Thus the preparatory epoch likelyrepresents a phase of movement preparation, during whichintegration of multiple signals can occur.

First, the spatial locus of attention has been shown to alterneural activity in area 7a and DP (Bender and Youakim 2001;Bushnell et al. 1981; Mountcastle et al. 1981; Quraishi et al.2007; Raffi and Siegel 2005; Steinmetz and Constantinidis1995). In the EVAR task, attention was overtly directed be-cause the reach target was always foveated, whereas in theRVAR task, attention was covertly directed to the nonfoveatedreach target (Bushnell et al. 1981; Quraishi et al. 2007; Stein-metz et al. 1994). Covert and overt attention are likely tomodulate neural responses during the RVAR and EVAR con-ditions, respectively. However, the variety of neural responsetypes suggests that the preparatory modulation went beyondmere attentional enhancement or suppression of the visualsignal (Sakata et al. 1995). Recent findings in lateral intrapa-rietal area (LIP) showed that motor planning and attentionalprocesses can be separated anatomically (Liu et al. 2010).Studies in PRR also strongly suggest that motor planning canbe distinguished from attentional modulation because it isdependent on the effector (Calton et al. 2002; Snyder et al.2006).

Second, this study also showed that motor planning likelycontributed to the preparatory signal through known anatomi-

FIG. 11. Proportions of interaction typebetween task condition (T) and position (P)plotted separately for each area (7a, filledbars; DP, open bars) for the preparatoryepoch (A) and the reach epoch (B). T-typeneurons had different firing rates betweentasks and flat spatial tuning. T�P-type neu-rons (multiplicative interaction) changedspatial tuning (response fields) betweentasks. NS cells had no effect of either factor.



cal feedforward and feedback pathways (Andersen 1997;Scherberger et al. 2005). It has been proposed that parietalcortex represents an early stage in movement planning (Snyderet al. 2000). Covert movement planning during a memory ordelay period modulates neurons in 7a (Snyder et al. 1997).Thus both area 7a and DP form part of a larger neural networkthat is crucial for transforming visual spatial information into amotor plan (Scherberger and Andersen 2007).

REACH RESPONSES. The firing rate during the reach epochlikely had both overt sensory and motor contributions, becausethe monkey detected the stimulus change, initiated the handmovement, and moved his hand toward the target. Changes inspatial tuning could derive from joint proprioception, becauseprimates are quite accurate in localizing their limbs in 3D spaceeven in absence of visual or tactile inputs (Baraduc et al. 2001;Ghika et al. 1995; Kalaska 1988; Prud’homme and Kalaska1994; Ren et al. 2006; Scheidt et al. 2005). Such inputs arelikely to be conveyed through other parietal areas that respondto somatosensory and proprioceptive manipulations (Breveg-lieri et al. 2006; Fattori et al. 2001; Ferraina et al. 1997, 2001;Johnson et al. 1996). An important contribution to the reachsignal could derive from efference copy or corollary discharge(Hyvärinen 1982; Mountcastle et al. 1975; Rushworth et al.1997). Indirect feedback from motor cortices through areas 7bor 5 might be involved in such signals (Gardner et al. 2007).These multiple signals are combined in time to monitor andmodulate ongoing reaching movements (Beurze et al. 2007).These modulatory signals likely propagate to DP through

strong reciprocal connections with area 7a and other parietaland frontal areas (Andersen et al. 1990a; Cavada and Gold-man-Rakic 1989b; Stepniewska et al. 2005). Thus this popu-lation of PPC neurons integrates information from multiplecortical sources to calculate the sensorimotor transformation.

Sensorimotor transformation and classification of neurons

The majority of studied area 7a and DP neurons modulatedtheir firing rate during the baseline, visual, preparatory, and/orreach epochs. Categorical regression methods were used toclassify neurons into different tuning types based on interac-tions between epoch and position. In the EVAR task, a smallproportion of neurons (�10%) were modulated by the epochbut were not spatially tuned (E-type cells). During the RVARtask, a slightly higher proportion of this tuning type was found.Large receptive fields that extend beyond the display couldexplain nonselectivity to retinotopic position. Overall, cells ofthis type for could reflect a gain signal from motor planning(Bullock et al. 1998; Snyder et al. 1998) or from nonspatialattentional modulation.

A substantial number of spatially tuned cells changed theirspatial preference (eye position tuning or retinotopic tuning)during progression of either task (E�P). During the EVARconditions, 59% of the neurons started with a certain eyeposition preference at baseline and stimulus onset and alteredtheir spatial tuning as the monkey prepared and executed hisreach movement. In the RVAR task, 45% changed their reti-notopic tuning. This suggests a predominance of gain field

FIG. 12. Response fields and spatial tuning of a typical area 7a (MJR050.C01; A, C, and E) and a DP neuron (MJR064.C02; B, D, and F). Preparatory epochduring EVAR and RVAR task (A and B): MJR050.C01 AEVAR � �0.068x � 0.45y � 0.003xy � 0.011y2 � 2.53; ARVAR � 0.19x � 0.33y � 0.024xy �0.021y2 � 2.53. MJR064.C02 AEVAR � �0.91x � 0.79y � 0.004xy � 0.12x2 � 21; ARVAR � �0.46x � 0.06y � 0.072xy � 0.012x2 � 21. Reach epoch duringEVAR and RVAR task (C and D). MJR050.C01 AEVAR � �0.24y � 0.009x2 � 1.78; ARVAR � 0.14y � 0.019x2 � 1.78. MJR064.C02 AEVAR � �0.98x �0.88y � 0.18y2 � 22.4; ARVAR � �0.49x � 0.47y � 0.057y2 � 22.4. Corresponding shifts in spatial preference (linear coefficients) between RVAR and EVARtasks for preparatory (gray arrows) and reach (black arrows) epochs (E and F).



tuning over retinotopic tuning in the population of neurons,which is in agreement with earlier studies (Heider et al. 2005;Read and Siegel 1997; Siegel et al. 2003). Substantial changesin spatial tuning occurred between the visual and preparatoryepoch for both conditions. These changes could arise fromspatially tuned attentional or planning signals based on othercoordinate frames (e.g., arm-centered, head-centered) originat-ing from frontal or other parietal areas (Pesaran et al. 2006;Rozzi et al. 2006). These signals modulated and changed theeye position and retinotopic tuning that prevailed during theearly “visual” phase of the task. Reach-related modulation,when the hand was lifted off the start position, could further beattributed to a combination of sensory (e.g., visual, proprio-ceptive) and motor signals as suggested for other parietal areas(Breveglieri et al. 2008).

Thus shifts in spatial tuning could represent highly specificfeedback from spatially tuned neurons in other cortical areas.Alternatively, initial generation or on-line modification of themotor command could arise within area 7a or DP to guide theensuing reach movement. Such motor commands need to begenerated in conjunction with visual information. This couldinvolve intracortical circuitry within area 7a and/or DP, con-sistent with lesion and imaging studies that support the role ofparietal cortex in on-line adjustment of reaching movementsunder visual control (Buxbaum and Coslett 1998; Desmurget etal. 1999; Pisella et al. 2000).

Contextual dependence of the sensorimotor transformations

To achieve accurate reaching performance, informationfrom various sources (e.g., visual, proprioceptive, efferencecopy) is updated continuously, allowing comparison of tar-geted with actual movement (Desmurget et al. 1998). Previousstudies have shown that gaze direction and retinotopic locationof a visual target modulate neural activity in both area 7a andDP neurons (Andersen et al. 1985, 1990a; Bremmer et al.1997; Heider et al. 2005; Read and Siegel 1997; Siegel et al.2003, 2007). To separate the contributions of retinotopic andgain field signals, the loci of fixation and retinal stimuli weresystematically varied and quantitatively assessed.

Behavioral effects of reaching to nonfoveated targets con-sisted of decreased reaching accuracy and shorter movementtimes, suggesting involvement of distinct neural populations.This also supports macro-level description of recruitment ofdifferent neural networks for foveal versus peripheral reachingassessed with event-related functional MRI and human lesionstudies (Clavagnier et al. 2007; Pisella et al. 2009). Behavioraldifferences between the tasks could also be caused by differ-ences in activity within the same population of neurons. Forexample, parietal area 5 cells combine signals from multiplesources to encode information about change of movementtrajectory (Archambault et al. 2009; Chen et al. 2009).

Human psychophysical findings support a strong couplingbetween gaze direction and pointing movements (Admiraal etal. 2004; Dijkerman et al. 2006; Henriques et al. 1998; Neggersand Bekkering 2001). When the gaze is held steady on thereach target, efference copy and ocular proprioception allowgreater accuracy in reaching (Lewis et al. 1998; Wilmut et al.2006). When the gaze is off the reach target, other sensorysignals such as arm proprioception exert a more prominentinfluence (Rossetti et al. 1995), which are likely to recruit

different neural populations. Visually guided reaching thusinvolves ongoing comparison of different sensory inputs (e.g.,visual vs. proprioceptive) to achieve maximum reach endpointaccuracy. Foveating the target could lead to longer movementtimes because of on-line corrective processes that combineocular and retinal signals (Bédard and Proteau 2004; Desmur-get and Grafton 2000). It has also been suggested that neuronsin parietal cortex use retinal error signal that reflect the differ-ence between target and hand position (Magescas et al. 2009).These error signals could be represented by PPC neuronsduring the different reach task conditions.

Direct comparisons of spatial tuning between RVAR andEVAR conditions during the preparatory and reach epochsshowed distinct populations of cells. Spatial tuning duringpreparation and initiation epochs differed between RVAR andEVAR conditions for about one half of all neurons (T�Pneurons). Task-related spatial changes in representations ofreach planning and execution have been described for otherparts of the cortex (Jouffrais and Boussaoud 1999; Schwartz etal. 1988). For example, motor cortex neurons are stronglyaffected by the kinetics of the arm movements (Scott andKalaska 1997; Scott et al. 1997). Because the movement timesin this study differed substantially between RVAR and EVARconditions, the trajectories were not identical between the twotask conditions.

These contextual effects can also be discussed with respectto different coordinate frames. Under both task conditions,reach movements were made to the same target locationrelative to the body (e.g., head, shoulders, or hands) but todifferent locations relative to the eye. If hand-centered signalsdominated the 7a and DP responses, the spatial tuning wouldbe similar between RVAR and EVAR conditions. If neuralresponses during reaching were dominated by eye-centeredsignals, spatial tuning would differ because eye position rela-tive to the reach target (i.e., hand position) varied betweenRVAR and EVAR tasks. This was the case for the majority ofcells, suggesting that eye position modulated tuning of thesecells during the preparation and initiation of the reach move-ment. The changes of spatial tuning over time (between ep-ochs) suggest that the initial eye position and retinotopic visualsignals are affected later during the task by other reach-relatedsignals. It is also likely that 7a and DP neurons use mixedcoordinate frames, for example, a combination of hand-cen-tered and eye-centered coordinates, as suggested for premotorand PRR neurons (Batista et al. 2007; Chang and Snyder2010).

Reach-related activity in dorsal prelunateand area 7a neurons

Neurons in area 7a are strongly visual but show substantialmodulation from extraretinal sources such as eye position(Andersen et al. 1990b; Read and Siegel 1997), attention(Constantinidis and Steinmetz 2001; Mountcastle et al. 1981;Quraishi et al. 2007; Raffi and Siegel 2005; Steinmetz andConstantinidis 1995; Steinmetz et al. 1994), and visuallyguided, goal-directed hand movements (Battaglia-Mayer et al.2007; MacKay 1992; Rozzi et al. 2008; Rushworth et al. 1997).

DP neurons also showed modulation during preparation andinitiation of reach movements, which was an unexpected resultof this study. Properties of DP neurons strongly resembled



those of area 7a with respect to temporal (epoch-based) andcontextual (task-related) effects. Thus these results support arole for DP neurons that goes beyond the merely visual(Fischer and Boch 1981a; Mountcastle et al. 1987; Tanaka etal. 1986). Although DP is lower in an anatomically definedhierarchy than area 7a (Andersen et al. 1990a; Felleman andVan Essen 1991), it receives modulatory feedback from otherparietal and frontal areas (Lewis and Van Essen 2000). Thepossibility that DP, and perhaps 7a, receive these signals viareentry (Edelman 1989) suggests a powerful role of theseprocesses.

A C K N O W L E D G M E N T S

We thank H. Poizner and M. Raffi for contributions and J. Siegel and R.Meltzer for technical assistance.

G R A N T S

This work was supproted by National Institutes of Health Grants EY-09223and 1S10 RR-12873, Whitehall Foundation, a Charles and Johanna BuschFaculty Research grant, and the National Partnership for Advanced Computa-tional Infrastructure.

D I S C L O S U R E S

No conflicts of interest, financial or otherwise, are declared by the authors.

R E F E R E N C E S

Admiraal MA, Keijsers NLW, Gielen CCAM. Gaze affects pointing towardremembered visual targets after a self-initiated step. J Neurophysiol 92:2380–2393, 2004.

Andersen RA. Multimodal integration for the representation of space in theposterior parietal cortex. Philos Trans R Soc Lond B Biol Sci 352: 1421–1428, 1997.

Andersen RA, Asanuma C, Essick G, Siegel RM. Corticocortical connec-tions of anatomically and physiologically defined subdivisions within theinferior parietal lobule. J Comp Neurol 296: 65–113, 1990a.

Andersen RA, Bracewell RM, Barash S, Gnadt JW, Fogassi L. Eyeposition effects on visual, memory, and saccade-related activity in areas LIPand 7a of macaque. J Neurosci 10: 1176–1196, 1990b.

Andersen RA, Essick GK, Siegel RM. Encoding of spatial location byposterior parietal neurons. Science 230: 456–458, 1985.

Andersen RA, Mountcastle VB. The influence of the angle of gaze upon theexcitability of the light- sensitive neurons of the posterior parietal cortex. JNeurosci 3: 532–548, 1983.

Andersen RA, Snyder LH, Bradley DC, Xing J. Multimodal representationof space in the posterior parietal cortex and its use in planning movements.Annu Rev Neurosci 20: 303–330, 1997.

Anderson KC, Siegel RM. Optic flow selectivity in the anterior superiortemporal polysensory area, STPa, of the behaving monkey. J Neurosci 19:2681–2692, 1999.

Archambault PS, Caminiti R, Battaglia-Mayer A. Cortical mechanisms foronline control of hand movement trajectory: the role of the posterior parietalcortex. Cereb Cortex 19: 2848–2864, 2009.

Baraduc P, Guigon E, Burnod Y. Recoding arm position to learn visuomotortransformations. Cereb Cortex 11: 906–917, 2001.

Batista AP, Andersen RA. The parietal reach region codes the next plannedmovement in a sequential reach task. J Neurophysiol 85: 539–544, 2001.

Batista AP, Buneo CA, Snyder LH, Andersen RA. Reach plans in eye-centered coordinates. Science 285: 257–260, 1999.

Batista AP, Santhanam G, Yu BM, Ryu SI, Afshar A, Shenoy KV.Reference frames for reach planning in macaque dorsal premotor cortex. JNeurophysiol 98: 966–983, 2007.

Batschelet E. Circular Statistics in Biology. London: Academic Press, 1981.Battaglia-Mayer A, Ferraina S, Genovesio A, Marconi B, Squatrito S,

Molinari M, Lacquaniti F, Caminiti R. Eye-hand coordination duringreaching. II. An analysis of the relationships between visuomanual signals inparietal cortex and parieto-frontal association projections. Cereb Cortex 11:528–544, 2001.

Battaglia-Mayer A, Mascaro M, Brunamonti E, Caminiti R. The over-representation of contralateral space in parietal cortex: a positive image ofdirectional motor components of neglect? Cereb Cortex 15: 514–525, 2005.

Battaglia-Mayer A, Mascaro M, Caminiti R. Temporal evolution andstrength of neural activity in parietal cortex during eye and hand movements.Cereb Cortex 17: 1350–1363, 2007.

Bédard P, Proteau L. On-line vs. off-line utilization of peripheral visualafferent information to ensure spatial accuracy of goal-directed movements.Exp Brain Res 158: 75–85, 2004.

Bender DB, Youakim M. Effect of attentive fixation in macaque thalamus andcortex. J Neurophysiol 85: 219–234, 2001.

Beurze SM, de Lange FP, Toni I, Medendorp WP. Integration of target andeffector information in the human brain during reach planning. J Neuro-physiol 97: 188–199, 2007.

Blum B. Manipulation reach and visual reach neurons in the inferior parietallobule of the rhesus monkey. Behav Brain Res 18: 167–173, 1985.

Bremmer F, Distler C, Hoffmann KP. Eye position effects in monkey cortex.II. Pursuit- and fixation-related activity in posterior parietal areas LIP and7A. J Neurophysiol 77: 962–977, 1997.

Breveglieri R, Galletti C, Gamberini M, Passarelli L, Fattori P. Somato-sensory cells in area PEc of macaque posterior parietal cortex. J Neurosci26: 3679–3684, 2006.

Breveglieri R, Galletti C, Monaco S, Fattori P. Visual, somatosensory, andbimodal activities in the macaque parietal area PEc. Cereb Cortex 18:806–816, 2008.

Bullock D, Cisek P, Grossberg S. Cortical networks for control of voluntaryarm movements under variable force conditions. Cereb Cortex 8: 48–62,1998.

Buneo CA, Jarvis MR, Batista AP, Andersen RA. Direct visuomotortransformations for reaching. Nature 416: 632–636, 2002.

Burnod Y, Baraduc P, Battaglia-Mayer A, Guigon E, Koechlin E, Fer-raina S, Lacquaniti F, Caminiti R. Parieto-frontal coding of reaching: anintegrated framework. Exp Brain Res 129: 325–346, 1999.

Bushnell MC, Goldberg ME, Robinson DL. Behavioral enhancement ofvisual responses in monkey cerebral cortex. I. Modulation in posteriorparietal cortex related to selective visual attention. J Neurophysiol 46:755–772, 1981.

Buxbaum LJ, Coslett H. Spatio-motor representations in reaching: evidencefor subtypes of optic ataxia. Cogn Neuropsychol 15: 279–312, 1998.

Calton JL, Dickinson AR, Snyder LH. Non-spatial, motor-specific activationin posterior parietal cortex. Nat Neurosci 5: 580–588, 2002.

Cavada C, Goldman-Rakic PS. Posterior parietal cortex in rhesus monkey. I.Parcellation of areas based on distinctive limbic and sensory corticocorticalconnections. J Comp Neurol 287: 393–421, 1989a.

Cavada C, Goldman-Rakic PS. Posterior parietal cortex in rhesus monkey.II. Evidence for segregated corticocortical networks linking sensory andlimbic areas with the frontal lobe. J Comp Neurol 287: 422–445, 1989b.

Chang SWC, Snyder LH. Idiosyncratic and systematic aspects of spatialrepresentations in the macaque parietal cortex. Proc Natl Acad Sci USA 107:7951–7956, 2010.

Chen J, Reitzen SD, Kohlenstein JB, Gardner EP. Neural representation ofhand kinematics during prehension in posterior parietal cortex of themacaque monkey. J Neurophysiol 102: 3310–3328, 2009.

Churchland MM, Santhanam G, Shenoy KV. Preparatory activity in pre-motor and motor cortex reflects the speed of the upcoming reach. JNeurophysiol 96: 3130–3146, 2006.

Clavagnier S, Prado J, Kennedy H, Perenin M-T. How humans reach:distinct cortical systems for central and peripheral vision. Neuroscientist 13:22–27, 2007.

Constantinidis C, Steinmetz MA. Neuronal responses in area 7a to multiple-stimulus displays. I. Neurons encode the location of the salient stimulus.Cereb Cortex 11: 581–591, 2001.

Coulthard EJ, Nachev P, Husain M. Control over conflict during movementpreparation: role of posterior parietal cortex. Neuron 58: 144–157, 2008.

Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE,Grafton ST. Role of the posterior parietal cortex in updating reachingmovements to a visual target. Nat Neurosci 2: 563–567, 1999.

Desmurget M, Grafton S. Forward modeling allows feedback control for fastreaching movements. Trends Cogn Sci 4: 423–431, 2000.

Desmurget M, Pelisson D, Rossetti Y, Prablanc C. From eye to hand:planning goal-directed movements. Neurosci Biobehav Rev 22: 761–788,1998.



Dijkerman HC, McIntosh RD, Anema HA, de Haan EHF, Kappelle LJ,Milner AD. Reaching errors in optic ataxia are linked to eye position ratherthan head or body position. Neuropsychologia 44: 2766–2773, 2006.

Edelman GM. The Remembered Present: A Biological Theory of Conscious-ness. New York: Basics Books, 1989.

Fattori P, Gamberini M, Kutz DF, Galletti C. ‘Arm-reaching’ neurons in theparietal area V6A of the macaque monkey. Eur J Neurosci 13: 2309–2313,2001.

Fattori P, Kutz DF, Breveglieri R, Marzocchi N, Galletti C. Spatial tuningof reaching activity in the medial parieto-occipital cortex (area V6A) ofmacaque monkey. Eur J Neurosci 22: 956–972, 2005.

Felleman DJ, Van Essen DC. Distributed hierarchical processing in theprimate cerebral cortex. Cereb Cortex 1: 1–47, 1991.

Ferraina S, Battaglia-Mayer A, Genovesio A, Marconi B, Onorati P,Caminiti R. Early coding of visuomanual coordination during reaching inparietal area PEc. J Neurophysiol 85: 462–467, 2001.

Ferraina S, Garasto MR, Battaglia-Mayer A, Ferraresi P, Johnson PB,Lacquaniti F, Carniniti R. Visual control of hand-reaching movement:activity in parietal area 7m. Eur J Neurosci 9: 1090–1095, 1997.

Fischer B, Boch R. Enhanced activation of neurons in prelunate cortex beforevisually guided saccades of trained rhesus monkeys. Exp Brain Res 44:129–137, 1981a.

Fischer B, Boch R. Selection of visual targets activates prelunate cortical cellsin trained rhesus monkey. Exp Brain Res 41: 431–433, 1981b.

Gardner EP, Babu KS, Reitzen SD, Ghosh S, Brown AS, Chen J, Hall AL,Herzlinger MD, Kohlenstein JB, Ro JY. Neurophysiology of prehension.I. Posterior parietal cortex and object-oriented hand behaviors. J Neuro-physiol 97: 387–406, 2007.

Ghika J, Bogousslavsky J, Uske A, Regli F. Parietal kinetic ataxia withoutproprioceptive deficit. J Neurol Neurosurg Psychiatry 59: 531–533, 1995.

Goldberg ME, Bisley J, Powell KD, Gottlieb J, Kusunoki M. The role of thelateral intraparietal area of the monkey in the generation of saccades andvisuospatial attention. Ann NY Acad Sci 956: 205–215, 2002.

Heider B, Jando G, Siegel RM. Functional architecture of retinotopy in visualassociation cortex of behaving monkey. Cereb Cortex 15: 460–478, 2005.

Henriques DYP, Crawford JD. Direction-dependent distortions of retinocen-tric space in the visuomotor transformation for pointing. Exp Brain Res 132:179–194, 2000.

Henriques DYP, Klier EM, Smith MA, Lowy D, Crawford JD. Gaze-centered remapping of remembered visual space in an open-loop pointingtask. J Neurosci 18: 1583–1594, 1998.

Hyvärinen J. The Parietal Cortex of Monkey and Man. Berlin: Springer-Verlag, 1982.

Johnson PB, Ferraina S, Bianchi L, Caminiti R. Cortical networks for visualreaching: physiological and anatomical organization of frontal and parietallobe arm regions. Cereb Cortex 6: 102–119, 1996.

Jouffrais C, Boussaoud D. Neuronal activity related to eye-hand coordinationin the primate premotor cortex. Exp Brain Res 128: 205–209, 1999.

Kalaska JF. The representation of arm movements in postcentral and parietalcortex. Can J Physiol Pharmacol 66: 455–463, 1988.

Kurata K, Hoshi E. Movement-related neuronal activity reflecting the trans-formation of coordinates in the ventral premotor cortex of monkeys. JNeurophysiol 88: 3118–3132, 2002.

Lewis JW, Van Essen DC. Corticocortical connections of visual, sensorimo-tor, and multimodal processing areas in the parietal lobe of the macaquemonkey. J Comp Neurol 428: 112–137, 2000.

Lewis RF, Gaymard BM, Tamargo RJ. Efference copy provides the eyeposition information required for visually guided reaching. J Neurophysiol80: 1605–1608, 1998.

Liu Y, Yttri EA, Snyder LH. Intention and attention: different functionalroles for LIPd and LIPv. Nat Neurosci 13: 495–500, 2010.

MacKay WA. Properties of reach-related neuronal activity in cortical area 7A.J Neurophysiol 67: 1335–1345, 1992.

Magescas F, Urquizar C, Prablanc C. Two modes of error processing inreaching. Exp Brain Res 193: 337–350, 2009.

Maguire WM, Baizer JS. Visuotopic organization of the prelunate gyrus inrhesus monkey. J Neurosci 4: 1690–1704, 1984.

Marzocchi N, Breveglieri R, Galletti C, Fattori P. Reaching activity inparietal area V6A of macaque: eye influence on arm activity or retinocentriccoding of reaching movements?. Eur J Neurosci 27: 775–789, 2008.

Merchant H, Battaglia-Mayer A, Georgopoulos AP. Effects of optic flow inmotor cortex and area 7a. J Neurophysiol 86: 1937–1954, 2001.

Moran DW, Schwartz AB. Motor cortical representation of speed anddirection during reaching. J Neurophysiol 82: 2676–2692, 1999.

Motter BC, Mountcastle VB. The functional properties of the light-sensitiveneurons of the posterior parietal cortex studied in waking monkeys: fovealsparing and opponent vector organization. J Neurosci 1: 3–26, 1981.

Mountcastle VB, Andersen RA, Motter BC. The influence of attentivefixation upon the excitability of the light-sensitive neurons of the posteriorparietal cortex. J Neurosci 1: 1218–1225, 1981.

Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C. Poste-rior parietal association cortex of the monkey: command functions foroperations within extrapersonal space. J Neurophysiol 38: 871–908, 1975.

Mountcastle VB, Motter BC, Steinmetz MA, Sestokas AK. Common anddifferential effects of attentive fixation on the excitability of parietal andprestriate (V4) cortical visual neurons in the macaque monkey. J Neurosci7: 2239–2255, 1987.

Neggers SFW, Bekkering H. Gaze anchoring to a pointing target is presentduring the entire pointing movement and is driven by a non-visual signal. JNeurophysiol 86: 961–970, 2001.

Pesaran B, Nelson MJ, Andersen RA. Dorsal premotor neurons encode therelative position of the hand, eye, and goal during reach planning. Neuron51: 125–134, 2006.

Pisella L, Grea H, Tilikete C, Vighetto A, Desmurget M, Rode G,Boisson D, Rossetti Y. An ‘automatic pilot’ for the hand in humanposterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 3:729–736, 2000.

Pisella L, Sergio L, Blangero A, Torchin H, Vighetto A, Rossetti Y. Opticataxia and the function of the dorsal stream: contributions to perception andaction. Neuropsychologia 47: 3033–3044, 2009.

Prablanc C, Pélisson D, Goodale MA. Visual control of reaching movementswithout vision of the limb. Exp Brain Res 62: 293–302, 1986.

Prud’homme MJ, Kalaska JF. Proprioceptive activity in primate primarysomatosensory cortex during active arm reaching movements. J Neuro-physiol 72: 2280–2301, 1994.

Quraishi S, Heider B, Siegel RM. Attentional modulation of receptive fieldstructure in area 7a of the behaving monkey. Cereb Cortex 17: 1841–1857,2007.

Raffi M, Siegel RM. Functional architecture of spatial attention in the parietalcortex of the behaving monkey. J Neurosci 25: 5171–5186, 2005.

Read HL, Siegel RM. Modulation of responses to optic flow in area 7a byretinotopic and oculomotor cues in monkey. Cereb Cortex 7: 647–661,1997.

Ren L, Khan AZ, Blohm G, Henriques DYP, Sergio LE, Crawford JD.Proprioceptive guidance of saccades in eye-hand coordination. J Neuro-physiol 96: 1464–1477, 2006.

Rossetti Y, Desmurget M, Prablanc C. Vectorial coding of movement:vision, proprioception, or both? J Neurophysiol 74: 457–463, 1995.

Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG, Matelli M,Luppino G. Cortical connections of the inferior parietal cortical convexityof the macaque monkey. Cereb Cortex 16: 1389–1417, 2006.

Rozzi S, Ferrari PF, Bonini L, Rizzolatti G, Fogassi L. Functional organi-zation of inferior parietal lobule convexity in the macaque monkey: elec-trophysiological characterization of motor, sensory and mirror responses andtheir correlation with cytoarchitectonic areas. Eur J Neurosci 28: 1569–1588, 2008.

Rushworth MF, Nixon PD, Passingham RE. Parietal cortex and move-ment. I. Movement selection and reaching. Exp Brain Res 117: 292–310,1997.

Sakata H, Taira M, Murata A, Mine S. Neural mechanisms of visualguidance of hand action in the parietal cortex of the monkey. Cereb Cortex5: 429–438, 1995.

Salinas E, Sejnowski TJ. Book review: gain modulation in the central nervoussystem: where behavior, neurophysiology, and computation meet. Neuro-scientist 7: 430–440, 2001.

Scheidt RA, Conditt MA, Secco EL, Mussa-Ivaldi FA. Interaction of visualand proprioceptive feedback during adaptation of human reaching move-ments. J Neurophysiol 93: 3200–3213, 2005.

Scherberger H, Andersen RA. Target selection signals for arm reaching inthe posterior parietal cortex. J Neurosci 27: 2001–2012, 2007.

Scherberger H, Goodale MA, Andersen RA. Target selection for reachingand saccades share a similar behavioral reference frame in the macaque. JNeurophysiol 89: 1456–1466, 2003.

Scherberger H, Jarvis MR, Andersen RA. Cortical local field potentialencodes movement intentions in the posterior parietal cortex. Neuron 46:347–354, 2005.

Schwartz A, Kettner R, Georgopoulos A. Primate motor cortex and free armmovements to visual targets in three- dimensional space. I. Relations



between single cell discharge and direction of movement. J Neurosci 8:2913–2927, 1988.

Scott SH, Kalaska JF. Reaching movements with similar hand paths butdifferent arm orientations. I. Activity of individual cells in motor cortex. JNeurophysiol 77: 826–852, 1997.

Scott SH, Sergio LE, Kalaska JF. Reaching movements with similar handpaths but different arm orientations. II. Activity of individual cells in dorsalpremotor cortex and parietal area 5. J Neurophysiol 78: 2413–2426, 1997.

Shadmehr R, Wise SP. The Computational Neurobiology of Reaching andPointing: A Foundation for Motor Learning. Cambridge, MA: MIT Press,2005.

Siegel RM, Duann JR, Jung TP, Sejnowski T. Spatiotemporal dynamics ofthe functional architecture for gain fields in inferior parietal lobule ofbehaving monkey. Cereb Cortex 17: 378–390, 2007.

Siegel RM, Raffi M, Phinney RE, Turner JA, Jando G. Functional archi-tecture of eye position gain fields in visual association cortex of behavingmonkey. J Neurophysiol 90: 1279–1294, 2003.

Siegel RM, Read HL. Analysis of optic flow in the monkey parietal area 7a.Cereb Cortex 7: 327–346, 1997.

Snyder LH, Batista AP, Andersen RA. Coding of intention in the posteriorparietal cortex. Nature 386: 167–170, 1997.

Snyder LH, Batista AP, Andersen RA. Change in motor plan, without achange in the spatial locus of attention, modulates activity in posteriorparietal cortex. J Neurophysiol 79: 2814–2819, 1998.

Snyder LH, Batista AP, Andersen RA. Intention-related activity in theposterior parietal cortex: a review. Vision Res 40: 1433–1441, 2000.

Snyder LH, Dickinson AR, Calton JL. Preparatory delay activity in themonkey parietal reach region predicts reach reaction times. J Neurosci 26:10091–10099, 2006.

Steinmetz MA, Connor CE, Constantinidis C, McLaughlin JR. Covertattention suppresses neuronal responses in area 7a of the posterior parietalcortex. J Neurophysiol 72: 1020–1023, 1994.

Steinmetz MA, Constantinidis C. Neurophysiological evidence for a role ofposterior parietal cortex in redirecting visual attention. Cereb Cortex 5:448–456, 1995.

Stepniewska I, Collins CE, Kaas JH. Reappraisal of DL/V4 boundariesbased on connectivity patterns of dorsolateral visual cortex in macaques.Cereb Cortex 15: 809–822, 2005.

Tanaka M, Weber H, Creutzfeldt OD. Visual properties and spatial distri-bution of neurones in the visual association area on the prelunate gyrus ofthe awake monkey. Exp Brain Res 65: 11–37, 1986.

Vercher JL, Magenes G, Prablanc C, Gauthier GM. Eye-head-hand coor-dination in pointing at visual targets: spatial and temporal analysis. ExpBrain Res 99: 507–523, 1994.

Wilmut K, Wann J, Brown J. How active gaze informs the hand in sequentialpointing movements. Exp Brain Res 175: 654–666, 2006.

Youakim M, Bender DB, Baizer JS. Vertical meridian representation on theprelunate gyrus in area V4 of macaque. Brain Res Bull 56: 93–100, 2001.

Zar JH. Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall, 1984.



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