Spatial computations underlying the coordination of the hand and eye present formidable geometric challenges. One way for the nervous system to simplify these computations is to directly encode the relative position of the hand and the center of gaze. Neurons in the dorsal premotor cortex (PMd), which is critical for the guidance of arm-reaching movements, encode the relative position of the hand, gaze, and goal of reaching movements. This suggests that PMd can coordinate reaching movements with eye movements. Here, we examine saccade-related signals in PMd to determine whether they also point to a role for PMd in coordinating visual–motor behavior. We first compared the activity of a population of PMd neurons with a population of parietal reach region (PRR) neurons. During center-out reaching and saccade tasks, PMd neurons responded more strongly before saccades than PRR neurons, and PMd contained a larger proportion of exclusively saccade-tuned cells than PRR. During a saccade relative position-coding task, PMd neurons encoded saccade targets in a relative position code that depended on the relative position of gaze, the hand, and the goal of a saccadic eye movement. This relative position code for saccades is similar to the way that PMd neurons encode reach targets. We propose that eye movement and eye position signals in PMd do not drive eye movements, but rather provide spatial information that links the control of eye and arm movements to support coordinated visual–motor behavior

Andersen, Richard A.

Nelson, Matthew J.

Pesaran, Bijan

English

Caltech Authors - Main

A relative position code for saccades in dorsal 
premotor cortex 
 
Bijan Pesaran, Matthew J. Nelson and Richard A. Andersen 
 
Supplementary Material 
Estimation bias in the statistical test for separability 
The idealized neuronal responses in Fig 2 show that separability is associated with a 
first singular value whose amplitude is large compared with the second singular value. It 
is difficult to establish statistical significance by directly comparing the amplitude of the 
first and second singular values as they are ordered amplitudes with the first singular 
value being necessarily larger than the second.  To avoid this problem, we defined 
separability by a significantly (p < 0.05) large first singular value compared to the first 
singular value calculated when trial conditions were randomized by permuting the rows 
and columns of the response matrix (Randomization test, 10,000 permutations).  Unlike 
permuting the trial labels and then recalculating the response matrix, permuting the rows 
and columns preserves the variability of the response matrix.   
 To test whether the above procedure for testing for separability is subject to 
estimation bias, we simulated the idealized neuronal responses for the six cases 
presented in Fig 2 as we varied the amount of data available for estimation.  We 
generated 3, 5, 10, 100, 1000 or 10000 simulated trials for each configuration by 
drawing the number of spikes in each trial from a Poisson distribution with a mean rate 
corresponding to  the value of the response matrix. The means were scaled so that the 
maximum firing rate in the response matrix was 50 Hz.  We then calculated the 
separability probability in each case.  Fig S1 presents the results.  We found that even 
shallow gain fields were reliably classified as separable (p < 0.05). This occurred with as 
few as three trials per condition and did not drastically change as the number of trials per 
condition increased to 10000.  In addition, the simulated vector response and both of the 
simulated intermediate responses were classified as inseparable (p > 0.05). Therefore, 
the procedure we used for determining separability is not subject to appreciable 
estimation bias and can reliably detect gain fields with as few as three trials per 
condition. 
 
Comparing PMd saccade responses with PRR saccade responses 
PRR neurons responded less before saccades than PMd neurons.  Across the 
population of 140 PRR neurons, we found 102 PRR cells were spatially tuned to either 
reaches or saccades.  This population included 90 cells (90/140; 64%, p<0.05) that were 
spatially tuned to reaches and 60 PRR cells (60/140; 43%, p<0.05) that were spatially 
tuned to saccades, albeit weakly at times.  As proportions of the 102 spatially tuned PRR 
cells, 42 cells (42/102; 41%) were exclusively tuned to reaches and not saccades, 12 
cells (12/102; 12%) were exclusively tuned to saccades not reaches, and 48 cells 
(48/102; 47%) were tuned to both reaches and saccades (see Table 1; Main text).  The 
48 PRR neurons (25 in Monkey E; 23 in Monkey Z) tuned to both reaches and saccades 
also had similar preferred directions for reaches and saccades with a mean difference of 
6° (Fig S2).  PRR neurons had a unimodal distribution of overall preferred directions that 
was peaked in the visual hemifield contralateral to the recording site (Rayleigh test, 
p<0.01). 
Our finding of strong a lateralization of the preferred directions of PRR neurons 
differs from earlier work studying the reach tuning of parietal neurons that shows a more 
uniform tiling of the workspace (Lacquaniti et al., 1995).  The difference in results may 
be due to two factors.  First, we recorded from PRR in the bank of the intraparietal 
sulcus, while earlier work has recorded from more superficial cortical regions on the 
gyrus of Brodmann’s Area 5.  Activity in the bank of the sulcus in the superior parietal 
lobule is more visual in nature than activity on the surface (Colby and Duhamel, 1991; 
Buneo and Andersen, 2006) and appears to be similar to area LIP on the lateral bank of 
the intraparietal sulcus, an area that shows strong lateralization of activity before 
saccades (Quian Quiroga et al., 2006),  Second, we made our recordings under 
enforced fixation while earlier recordings from Area 5 were done during free-gaze. The 
activity of parietal neurons is centered on the orientation of gaze (Batista et al., 1999; 
Buneo et al., 2002; Pesaran et al., 2006), and changes in eye position during freely-
made eye movements has been shown to affect the responses of parietal neurons that 
are active before reaches (Cisek and Kalaska, 2002). 
 
Comparing the spatial reference frame for saccades and reaches 
In a previous study (Pesaran et al., 2006), we recorded from PMd and PRR neurons 
while monkeys performed a reach relative position coding task (Fig S3). This task was 
identical to the saccade relative position coding task in the present study, with the 
exception that it required a reach instead of a saccade. Before reaches, we had 
previously found that individual PMd neurons were spatially tuned to multiple vectors, 
TG, HG and TH,   We had also found that the strength of spatial tuning to these vectors 
was equal (Pesaran et al., 2006).  Figure S4 presents the reach data for comparison 
with the saccade data presented in the main text (Fig 10).  The number of PMd cells 
with tuned, inseparable responses to TG, TH and HG before reaches and their 
intersections are shown in a Venn diagram (Fig S4A).  Cells tended to encode a mixture 
of tuning to more than one vector and many encoded all three vectors.  This pattern was 
mirrored in the strength of tuning to each vector.  Examining the tuning strength of the 
response matrices using the length of the resultant of the gradient analysis revealed that 
before reaches, PMd neurons encode all three vectors, TG, TH and HG, with equal 
strength (Fig S4B). These data stand in contrast to the responses of PMd cells during 
the saccade relative position coding task (Fig 10), in which cells were more likely to 
encode only one of the vectors, and tended to code the vector HG the strongest, followed 
by TH and then TG. Thus the spatial encoding scheme for saccades and reaches are 
mostly similar in PMd, albeit with some differences. 
    
Tuning to hand and gaze position during baseline 
The strength of relative hand-gaze encoding suggests PMd neurons may also encode 
the position of the hand and/or gaze in the absence of a plan to move.  This signal could 
maintain postural information which could then be combined with incoming target 
information to plan movements.  To investigate this representation, we analyzed how 
activity during the baseline period of the task before target presentation depended on the 
static position of the hand and gaze.  Using the matrix analysis, we found that the activity 
of many PMd cells was tuned to hand and gaze position during the baseline before a 
saccade (53/116; 46%; p<0.05 randomization test).    A similar fraction of PMd cells was 
tuned to hand and gaze position during the baseline before a reach (51/111; 46%; 
p<0.05) and these two proportions were not significantly different (p=0.70; Two-sample 
binomial test).  The resultant of the gradient analysis showed that the strength of tuning 
of baseline activity in each task was also not significantly different (Reach baseline 
tuning strength:  p=0.87; Rank-sum test).  This shows that baseline tuning to gaze and 
hand position is widespread in PMd neurons and is not influenced by whether a saccade 
or reach movement will follow. 
 Baseline response matrices of PMd neurons showed diagonal more than 
horizontal or vertical structure. HG position response matrices for individual cells peaked 
when either the hand was ipsilateral to the eye (Fig S5A), as well as when the hand was 
on the eye, or the hand was contralateral to the eye.  For the population of PMd cells 
tuned during the baseline period, baseline tuning for hand position could not be 
separated from gaze position for a majority of cells (Fig S5B. 43/53; 82%) inseparable; 
p>0.05, bootstrap test).  We found that inseparable PMd cells encoded the difference 
between hand and gaze position with a mean response field orientation -86° (Fig S5C).   
 These analyses indicate that the activity of PMd neurons is affected by moving 
the hand to the left as much as by moving gaze to the right, and vice versa.  
Interestingly, the level of activity at the peak of the response field was greater when the 
hand was ipsilateral to gaze than when the hand was contralateral to gaze (p<0.05, 
Rank-sum test).  This means cells in PMd prefer the hand ipsilateral to gaze.  We 
observed the same relative hand-gaze position preference in both the reach and 
saccade relative position coding tasks.  Cells which preferred the hand ipsilateral to gaze 
in the reach task, tended to also prefer the hand ipsilateral to gaze in saccade task (Fig 
S6). This configuration of hand and eye position is more common during behavior and is 
consistent with reports of a preference for gaze centered with respect to the body 
(Scherberger et al., 2003).  Therefore, preferred relative hand-gaze position of individual 
neurons in PMd may match the statistics of natural behavior. 
 
References 
Batista, A. P., Buneo, C. A., Snyder, L. H., and Andersen, R. A. (1999). Reach plans in 
eye-centered coordinates. Science 285, 257-260. 
 
Buneo, C. A., and Andersen, R. A. (2006). The posterior parietal cortex: sensorimotor 
interface for the planning and online control of visually guided movements. 
Neuropsychologia 44, 2594-2606. 
 
Buneo, C. A., Jarvis, M. R., Batista, A. P., and Andersen, R. A. (2002). Direct visuomotor 
transformations for reaching. Nature 416, 632-636. 
 
Cisek, P., and Kalaska, J. F. (2002). Modest gaze-related discharge modulation in 
monkey dorsal premotor cortex during a reaching task performed with free 
fixation. J. Neurophysiol 88, 1064-1072. 
 
Colby, C. L., and Duhamel, J. R. (1991). Heterogeneity of extrastriate visual areas and 
multiple parietal areas in the macaque monkey. Neuropsychologia 29, 517-537. 
 
Lacquaniti, F., Guigon, E., Bianchi, L., Ferraina, S., and Caminiti, R. (1995). 
Representing spatial information for limb movement: role of area 5 in the 
monkey. Cereb. Cortex 5, 391-409. 
 
Pesaran, B., Nelson, M. J., and Andersen, R. A. (2006). Dorsal premotor neurons 
encode the relative position of the hand, eye, and goal during reach planning. 
Neuron 51, 125-134. 
 
Quian Quiroga, R., Snyder, L. H., Batista, A. P., Cui, H., and Andersen, R. A. (2006). 
Movement intention is better predicted than attention in the posterior parietal 
cortex. J. Neurosci 26, 3615-3620. 
 
Figure Captions 
 
Figure S1  Assessment of estimation bias in the procedure for calculating separability.  
The probability of separability is plotted as the number of trials per condition from three 
to 1000 trials for each of the six idealized neuronal responses shown in Fig 2.  
Intermediate I presents results for the response shown in Fig 2B.  Intermediate II 
presents results for the response shown in Fig 2C. For display purposes, we added 10-4 
to the medium gain field results and 2x10-4 to the shallow gain field results. Dotted line 
shows p=0.05 level used for establishing significance. 
 
Figure S2  Population histogram of difference in preferred directions during delay 
periods before saccades and reaches for PRR neurons. Asterisk marks the mean 
preferred direction difference.  Preferred directions before a reach and saccade point in 
similar directions.   
 
 
Figure S3  Reach relative position coding task.  A reach is made from one of four initial 
hand positions on a line to one of four target positions while gaze is maintained at one of 
four gaze positions. Hand positions and reach targets are shown in green, gaze 
positions are shown in red. 
 
Figure S4  PMd delay period responses during the reach relative position coding task.  
(a)  Venn diagram of the number of neurons with tuned inseparable TG, HG and TH 
responses during the reach relative position coding task.  (b)  Tuning strength of the 
reach response matrices.  * denotes significant difference (p<0.05). 
 
Figure S5 Hand and gaze (HG) tuning during the baseline period of the saccade relative 
position coding task.   (a) Example PMd neuron response.  The PMd example cell from 
Figure 7 (main text) is shown.  Numbers denote average firing rate for each hand-gaze 
combination.  (b)  Population HG separability for PMd neurons.  (c)  Population HG 
response field orientation for PMd neurons. Orientations for separable cells are shown in 
dark grey.  Orientations for inseparable cells are shown in light grey. Similar responses 
were seen during the baseline period of the reach    
 
Figure S6  Relative hand-eye position preference during the baseline period for neurons 
recorded in both reach and saccade reference frame tasks.  The number of neurons with 
a preference for the hand ipsilateral to the eye, aligned with the eye or contralateral to 
the eye is shown for each task. 
 
100 101 102 103 104
10-4
10-3
10-2
10-1
100
P
ro
ba
bi
lit
y
Number of trials per condition
Moderate Gain Field
Weak Gain Field
Strong Gain Field
Vector
Intermediate I
Intermediate II
Figure S1
-180 -90 0 90 180
0
5
10
15
20 *
N
um
be
r o
f c
el
ls
Figure S2
Difference in
delay tuning for reach 
and saccade
PRR
Reach relative position coding task
Figure S3
...
...
TG
HG TH
6 5 10
16
713
6
A
Figure S4
Reach Relative Position Coding
TG HG TH
Vector
0
1
0.5
Tu
ni
ng
 S
tre
ng
th
 
(H
z/
de
gr
ee
)
B
AFigure S5
PMd PopulationPMd cell
-20 -10 0 10
-20
-10
0
10
1
35
70 Hz
Hand
Gaze
53 71 72 33
50 52 37 2
69 33 4 3
32 7 9 3
N
um
be
r o
f c
el
ls
0
25
50
Sep Insep
HG
H-G
H+G
B C
10
20
9 cells34
5 52
3 1
Saccade
Task
Reach
Task
HCE
HIE
HIEHCE
HCE: Hand contrato eye
Hand ipsi
to eyeHIE:
Figure S6
1


A Relative Position Code for Saccades in Dorsal Premotor Cortex

Direct visuomotor transformations for reaching.

Dorsal premotor neurons encode the relative position of the hand, eye, and goal during reach planning.

Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey.

Modest gaze-related discharge modulation in monkey dorsal premotor cortex during a reaching task performed with free fixation.

Movement intention is better predicted than attention in the posterior parietal cortex.

Reach plans in eye-centered coordinates.

Representing spatial information for limb movement: role of area 5 in the monkey.

The posterior parietal cortex: sensorimotor interface for the planning and online control of visually guided movements.

https://authors.library.caltech.edu/18516/1/Pesaran2010p10160J_Neurosci.pdf

A Relative Position Code for Saccades in Dorsal Premotor Cortex

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