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<article article-type="research-article" xmlns:xlink="http://www.w3.org/1999/xlink">
  <front>
    <journal-meta>
	<journal-id journal-id-type="publisher-id">Jemr</journal-id>
      <journal-title-group>
        <journal-title>Journal of Eye Movement Research</journal-title>
      </journal-title-group>
      <issn pub-type="epub">1995-8692</issn>
	  <publisher>								
	  <publisher-name>Bern Open Publishing</publisher-name>
	  <publisher-loc>Bern, Switzerland</publisher-loc>
	</publisher>
    </journal-meta>
    <article-meta>
      <article-id pub-id-type="doi">10.16910/jemr.10.3.6</article-id>
       <article-categories>								
				<subj-group subj-group-type="heading">
					<subject>Research Article</subject>
				</subj-group>
		</article-categories>
	  <title-group>
        <article-title>Interference between smooth pursuit and color working memory</article-title>
      </title-group>
      <contrib-group>
	    
				<contrib contrib-type="author">
					<name>
						<surname>Yue</surname>
						<given-names>Shulin</given-names>
					</name>
					<xref ref-type="aff" rid="aff1">1</xref>
				</contrib>

      				<contrib contrib-type="author">
					<name>
						<surname>Jin</surname>
						<given-names>Zhenlan</given-names>
					</name>
					<xref ref-type="aff" rid="aff2">2</xref>
				</contrib>		
		  
		  
	 
				<contrib contrib-type="author">
					<name>
						<surname>Chenggui</surname>
						<given-names>Fan</given-names>
					</name>
					<xref ref-type="aff" rid="aff1">1</xref>
				</contrib>
		
		
		
				<contrib contrib-type="author">
					<name>
						<surname>Qian</surname>
						<given-names>Zhang</given-names>
					</name>
					<xref ref-type="aff" rid="aff1">1</xref>
				</contrib>			<contrib contrib-type="author">
					<name>
						<surname>Li</surname>
						<given-names>Ling</given-names>
					</name>
					<xref ref-type="aff" rid="aff2">2</xref>
				</contrib>
				
				
	
		
		
		
        <aff id="aff1">
          <label>1</label>
          <institution>University of Electronic Science and Technology of China</institution>
          ,
          <addr-line>Chengdu</addr-line>
          ,
          <country country="CN">China</country>
        </aff>
     
  
        <aff id="aff2">
          <label>2</label>
          <institution>Key Laboratory for NeuroInformation of Ministry of Education, University of Electronic Science and Technology of China</institution>
          ,
          <addr-line>Chengdu</addr-line>
          ,
          <country country="CN">China</country>
        </aff>
      </contrib-group>
      
	  
	  
	  
	  
	  
	  <pub-date date-type="pub" publication-format="electronic"> 
		<day>10</day>  
		<month>7</month>
        <year>2017</year>
      </pub-date>
	  <pub-date date-type="collection" publication-format="electronic"> 
	  <year>2017</year>
	</pub-date>
      <volume>10</volume>
      <issue>3</issue>
	  <elocation-id>10.16910/jemr.10.3.6</elocation-id>
	<permissions> 
	<copyright-year>2017</copyright-year>
	<copyright-holder>Yue et al.</copyright-holder>
	<license license-type="open-access">
  <license-p>This work is licensed under a Creative Commons Attribution 4.0 International License, 
  (<ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">
    https://creativecommons.org/licenses/by/4.0/</ext-link>), which permits unrestricted use and redistribution provided that the original author and source are credited.</license-p>
</license>
	</permissions>
      <abstract>
        <p>Spatial working memory (WM) and spatial attention are closely related, but the relationship between non-spatial WM and spatial attention still remains unclear. The present study aimed to investigate the interaction between color WM and smooth pursuit eye movements. A modified delayed-match-to-sample paradigm (DMS) was applied with 2 or 4 items presented in each visual field. Subjects memorized the colors of items in the cued visual field and smoothly moved eyes towards or away from memorized items during retention interval despite that the colored items were no longer visible. The WM performance decreased with higher load in general. More importantly, the WM performance was better when subjects pursued towards rather than away from the cued visual field. Meanwhile, the pursuit gain decreased with higher load and demonstrated a higher result when pursuing away from the cued visual field. These results indicated that spatial attention, guiding attention to the memorized items, benefits color WM. Therefore, we propose that a competition for attention resources exists between color WM and smooth pursuit eye movements.</p>
      </abstract>
      <kwd-group>
        <kwd>color WM</kwd>
        <kwd>smooth pursuit</kwd>
        <kwd>spatial attention</kwd>
        <kwd>retention period</kwd>
        <kwd>delayed-matchto-sample paradigm</kwd>
        <kwd>dual-task</kwd>
      </kwd-group>
    </article-meta>
  </front>
    <body>
  <sec id="s1">
      <title>Introduction</title>
      <p>Working memory (WM)
        <xref ref-type="bibr" rid="b5 b6 b12">(Baddeley, 2000; Baddeley
&amp; Hitch, 1974; Engle, 2002)</xref>facilitates temporary
maintenance of relevant information in the mind and
plays a critical role in many complex cognitive tasks.
Visual WM stores and manipulates visual and spatial
information and these information are stored relatively
separate within the visuospatial sketchpad
        <xref ref-type="bibr" rid="b5">(Baddeley,
2000)</xref>
        . Spatial WM and spatial attention are closely
related
        <xref ref-type="bibr" rid="b3 b9">(Awh &amp; Jonides, 2001; Cowan, 2000)</xref>
        and spatial
attention plays an important role in maintaining location
information
        <xref ref-type="bibr" rid="b3">(Awh &amp; Jonides, 2001)</xref>
        .
      </p>
      
	  
	  <p>
        As widely accepted, spatial attention and eye
movements are intimately coupled
        <xref ref-type="bibr" rid="b33 b35 b22 b23 b24 b29">(Posner, 1980; Reeves &amp;
Sperling, 1986; Kurylo, Reeves, &amp; Scharf, 1996; Kowler,
Anderson, Dosher &amp; Blaser, 1995; Kustov &amp; Robinson,
1996; Moore &amp; Fallah, 2004)</xref>
        . Shift of spatial attention
can be overt or covert and eye movements demonstrate
overt shift of spatial attention. Therefore, it is natural that
eye movements interact with spatial WM. Refixations on
an object when freely inspecting a scene improve the
memory performance and it was proposed that refixations
continuously update the availability of items in the
memory
        <xref ref-type="bibr" rid="b47">(Zelinsky &amp; Loschky, 2009)</xref>
        . On the contrary,
there are also studies demonstrating the interference of
eye movements on the spatial WM
        <xref ref-type="bibr" rid="b39 b19">(Baddeley &amp;
Lieberman, 1980; Kerzel &amp; Ziegler, 2005; Smyth &amp; Scholey,
1994)</xref>
        . In line with the close relationship between spatial
WM and attention,
        <xref ref-type="bibr" rid="b25">Lawrence, Myerson, and Abrams
(2004</xref>
        ) found that the spatial WM span was decreased by
the covert shift of attention and even more by eye
movements, demonstrating that eye movements interfere with
spatial WM and the interference caused by eye
movements is greater than covert attention shift. Moreover,
keeping a location in memory curved eye trajectories
away from the remembered location
        <xref ref-type="bibr" rid="b44">(Theeuwes, Olivers,
&amp; Chizk, 2005)</xref>
        . These studies demonstrate an intimate
link between the control of eye movements, attention and
working memory
        <xref ref-type="bibr" rid="b15 b43">(Golomb, Chun, &amp; Mazer, 2008;
Theeuwes, Belopolsky, &amp; Olivers, 2009)</xref>.</p>
      <p>In contrast with the clear relationship between spatial
WM and eye movements, the relationship between eye
movements and non-spatial WM is still under debate. In
the study of
        <xref ref-type="bibr" rid="b4">Awh, Jonides, and Reuter-Lorenz (1998</xref>
        ), a
letter appeared and subjects had to memorize the location
of the letter or the identity of the letter. At the same time,
choice stimuli appeared during the retention interval and
subjects indicated the shape of the stimuli by pressing
button quickly. Reaction times to choice stimuli were
faster if they appeared at the memorized location,
suggesting that spatial attention is focused on the memorized
location. In contrast, when remembering the identity of
the letter, no benefit of the location of the letter was
observed, suggesting the specific relation between spatial
WM and visual attention. Similarly, in the study of
        <xref ref-type="bibr" rid="b25">Lawrence, Myerson, and Abrams (2004</xref>
        ), the authors found a
reduction in the spatial WM span by the attention shift,
but not in the verbal WM. In line with these findings, a
movement discrimination task interferes with the spatial
WM task of memorizing dot locations, while a color
discrimination task does not
        <xref ref-type="bibr" rid="b21">(Klauer &amp; Zhao, 2004)</xref>
        .
Additionally,
        <xref ref-type="bibr" rid="b19">Kerzel and Ziegler (2005)</xref>
        found that the color WM performance was unaffected by the addition of
smooth pursuit task while the spatial WM performance was impaired by the additional smooth pursuit task. On
the contrary,
        <xref ref-type="bibr" rid="b28">Makovski and Jiang (2009)</xref>
        found
concurrent performance of a color WM task and attentive
tracking task produced mutual interference with each other. In
their study, subjects were encouraged to maintain fixation
at the display center while attentively tracking multiple
objects. They proposed that common attentional
processes are engaged in these two tasks which are of central and
amodal origin.
        <xref ref-type="bibr" rid="b5">Baddeley (2000)</xref>
        proposed a multiple
component model, which included central executive,
visuospatial sketchpad, phonological loop and episodic
buffer. Furthermore, visual and spatial information were
stored relatively separately within the visuospatial
sketchpad. Therefore, we assumed that the common
attentional resources shared by attentive tracking and color
WM point to the central executive component in
Baddeley&#x2019;s model (2000).</p>
      
	  
	  <p>Similar to the intimate couple of visual spatial
attention and saccades, smooth pursuit eye movements foveate
moving objects and are closely related to visual attention
as well. Dividing attention from the smooth pursuit could
impair the pursuit performance
        <xref ref-type="bibr" rid="b1 b7 b16 b41">(Acker &amp; Toone, 1978;
Brezinova &amp; Kendell, 1977; Heinen, Jin, &amp; Watamaniuk,
2011; Souto &amp; Kerzel, 2008)</xref>
        . Addition of larger random
dot cinematogram (RDC) that moves with the pursuit
target helps to release attention from the pursuit which
can be used to improve performance of secondary
attention task
        <xref ref-type="bibr" rid="b17">(Jin et al., 2013)</xref>
        . These results demonstrate that
attention is involved in the smooth pursuit eye
movements. In addition, studies showed that attention is
narrowly allocated around the smooth pursuit target although
with some conflicts. Some studies showed that attention
allocation during smooth pursuit is asymmetric, more
attention is distributed ahead of the pursuit target
        <xref ref-type="bibr" rid="b18 b20 b37 b38 b45">(Kanai,
van der Geest, &amp; Frens, 2003; Khan, Lefe`vre, Heinen, &amp;
Blohm, 2010; Seya &amp; Mori, 2012; Smeets &amp; Bekkering,
2000; van Donkelaar &amp; Drew, 2002)</xref>
        , while others
proposed that attention is symmetrically distributed around
the pursuit target
        <xref ref-type="bibr" rid="b26 b46">(Lovejoy et al., 2009; Watamaniuk &amp;
Heinen, 2015)</xref>
        . Studies on schizophrenia demonstrated
that spatial WM impairment was associated with
dysfunctions in the oculomotor mechanisms
        <xref ref-type="bibr" rid="b30 b40">(Park &amp;
Holzman, 1993; Snitz et al, 1999)</xref>
        . The deficit of spatial
WM performance was related to smooth pursuit because
of the limitation of attention distributed to position
        <xref ref-type="bibr" rid="b19 b30 b31">(Kerzel &amp; Ziegler, 2005; Park, Holzman, &amp; Levy, 1993)</xref>
        .
However, color WM performance was unaffected by the
addition of smooth pursuit task, suggesting the allocation
of attention was restricted to position which is
responserelevant dimension
        <xref ref-type="bibr" rid="b19">(Kerzel &amp; Ziegler, 2005)</xref>
        . These
studies again implied the ambiguity of the relationship
between eye movements and non-spatial WM.</p>
	  
	  
	  
	  
	  
      <p>Therefore, we designed a delayed-match-to-sample
paradigm (DMS), whereby a WM load task is interleaved
with pursuit task during the maintenance period in the
present study. In the experiment, subjects memorized the
color of squares in the cued visual field and foveated a
moving cross during the retention period. The cross
moved toward or away from the visual field where the
memory targets were presented. Since attention is
narrowly distributed around the pursuit target, pursuing
towards or away from the cued visual field might
influence the color WM differently because the attention
would be allocated in the cued VF or in the uncued VF in
the present design. Therefore, we asked whether eye
movements affect the performance of color WM and
whether smoothly directing gaze toward or away from the
previous location of the memory item would have
differential effects on the color WM.</p>
    </sec>
	<sec id="s2">
      <title>Methods</title>
      <sec id="s2a">
        <title>Participants</title>
        <p>Sixteen college students (five females and eleven
males, mean age 22.8) with normal vison participated in
the experiment. All subjects had no history of
neurological diseases and were completely na&#xEF;ve to the aim of the
current study. The study was approved by the University
of Electronic Science and Technology of China Ethics
Board and the methods were performed in accordance
with the approved guidelines and all experiments
conformed to the declaration of Helsinki. All subjects signed
written consent form before participating in the study.</p>
      </sec>
      <sec id="s2b">
        <title>Apparatus and visual stimuli</title>
        <p>The stimuli were generated by Psychtoolbox
          <xref ref-type="bibr" rid="b32">(Pelli,
1997)</xref>
          in MATLAB and were presented on a 1024&#xD7;768
pixels display with a refresh rate of 60 Hz. Eye
movement data were recorded by EyeLink1000plus eye-tracker
(SR Research Ltd., Kanata, Canada) with sampling rate
of 2000 Hz. The tracker was calibrated and validated
through the way in which the observer fixated nine
locations distributed across the display using a standard
software routine provided with the EyeLink system. Subjects
were seated on a chair in darkness with their head
stabilized using a chin and forehead rest and viewed the
stimuli display from a distance of 65cm.</p>
        <p>Colors of the WM stimuli were made by adobe
fireworks with uniform luminance, saturation and resolution.
There were nine colors to be picked. Each colored square
was 0.88 degree in width and could be presented at one of
four potential locations in each visual field. The colored
squares were arranged along imaginary lines which were
displaced 3.86 degree to the left and right of fixation and
the vertical distance between squares was 0.88 degree.</p>
      </sec>
      <sec id="s2c">
        <title>Procedure</title>
        <p>The study included three sessions, the WM + pursuit
session, the WM-only session and pursuit-only session.
The WM-only session and pursuit-only session is
basically same as the WM + pursuit session, so we will describe
this session as a representative in details below. Each trial
began with a random duration (500-1000 ms) of central
cross (0.49 degree in length), which was followed by a
300 ms cue (0.49 degree in length) pointing to left or
right with equal probability. The WM target stimuli
appeared after the cue and stayed on the display for 500 ms.
The target stimuli consisted of 2 or 4 colored squares in
both left and right visual fields (VFs) in addition to the
central cross <xref ref-type="fig" rid="fig01">Figure 1</xref>. In trials with 4 squares (load 4
condition), the squares were presented at all four possible
locations in each visual field. Meanwhile, in trials with 2
squares (load 2 condition), the squares were always
presented at two locations near the horizontal meridian in
each visual field. These constant positions of squares in
each condition were aimed to diminish the potential
effect of location change across trials. At the same time of
the target stimuli offset, the fixation cross jumped back
0.88 degree and moved for 1500 ms towards the left or
the right visual field at the constant velocity of 5.26
deg/s. The backward 0.88 degree step contributed to
reduce the occurrence of catch-up saccades <xref ref-type="bibr" rid="b34">(Rashbass,
1961)</xref>. The motion direction of the cross was consistent
or inconsistent with the cue direction and each type
occupied 50% of trials. This manipulation generated four
types of trials, each type occupied a quarter of trials.
After the moving cross disappeared, the test stimuli were
presented and stayed on the display until the response.
Colors of the squares in the cued VF of the test stimuli
were either same as those in the cued VF of the target
stimuli or one of them changed its color. Similarly, the
colors in the uncued VF of the test stimuli were same as
those in the uncued VF of the target stimuli or one of
them changed its color with equal chance. The change of
square colors in the cued and uncued VF were
independent each other. As soon as the test stimuli appeared,
subjects were instructed to click the left (Yes) or right (No)
button of the mouse quickly to indicate whether the
colors in the cued VF changed or not with maximum time
window of 3 seconds.</p>

<fig id="fig01" fig-type="figure" position="float">
					<label>Figure 1</label>
					<caption>
						<p>Schematic representation of stimuli sequence in
the WM + pursuit session. The cue pointed to the left and right
before the onset of the target stimuli, which consisted of 2 or 4
colored squares in both VFs. Subjects were required to memorize
the color of the squares in the cued VF and judged whether
the colors of the test stimuli in the cued VF were same or not.
During the retention period, subjects pursued the cross which
moved towards or away from the cued VF. According to the
direction of the cross motion, the trials were grouped into consistent
and inconsistent trials.</p>
					</caption>
					<graphic id="graph01" xlink:href="jemr-10-03-f-figure-01.png"/>
				</fig>



        <p>The WM-only session was same as the WM + pursuit
session except that the central cross was static and stayed
at the display center during the retention period. Subjects
conducted the WM task as in the WM + pursuit session
and fixated at the central cross during the retention
period. In the pursuit-only session, both the target and test
stimuli for the WM task were not presented during the
target presentation period and test stimuli period, but only
the central cross.</p>


        <p>Subjects practiced the pursuit task until they could
pursue smoothly before collecting the data. Each subject
completed 4 blocks of the main experiment (WM and
pursuit dual-task) and 2 blocks of each control
experiment. All blocks in the study had 64 trials, so each
subject produced 512 trials in total.</p>

      </sec>
      <sec id="s2d">
        <title>Data analysis</title>
        <p>Eye movement data were analyzed offline. Horizontal
and vertical eye velocities were calculated offline from
the recorded position signals by differentiating and
filtering (2-pole Butterworth noncausal filter, cutoff = 50 Hz).
Saccade detection used an empirically-chosen threshold
of 25&#xB0;/s. For the pursuit data analysis, the open-loop
period was considered to have a duration of 150 ms, with
an onset of 150 ms after the stimuli motion onset
(average pursuit latency over all subjects was 152 ms).
Openloop gain was computed by dividing average eye velocity
over a 20 ms bin centered 300 ms after the stimuli motion
onset (the end of open-loop period) by stimuli velocity.
Steady-state gain was computed by dividing mean eye
velocity in a 450-950 ms time window by stimuli
velocity.</p>
        <p>Trials with failure of eye position recording or with
blink which occurred from the cue onset to the end of
motion, were excluded from the analysis. In addition,
trials with eyes deviating from the fixation more than 2o
during the last 100 ms of the target stimuli presentation
were discarded as well to assure the starting position of
the pursuit. After these trial removals, 88.82% of trials
survived on average in all subjects.</p>
      </sec>
    </sec>
	
	 <sec id="s3">
      <title>Results</title>
      <p>First, we compared the WM performance in the WM
+ pursuit session and the WM-only session to investigate
whether adding secondary pursuit task in the retention
period would harm the WM performance. To do this, we
have conducted a two-way repeated-measure ANOVA
using the WM load (load 2 and 4) and the presence of
pursuit task (without and with pursuit task) as factors
<xref ref-type="fig" rid="fig02">Figure 2</xref>. As usual, we found the WM accuracy
decreased with higher load (F(1,15)=270.97, p=0.000) and
adding the pursuit task did reduce the WM accuracy
(F(1,15)=9.27, p=0.008). Consistently, the reaction times
were longer with higher load (F(1,15)=11.94, p=0.004)
and adding the pursuit task lengthened the reaction times
(F(1,15)=4.83, p=0.044) as well. These results
demonstrated that eye movements during the retention period
harmed the WM performance.</p>


<fig id="fig02" fig-type="figure" position="float">
					<label>Figure 2</label>
					<caption>
						<p>The WM performance with and without pursuit
task. Light grey indicates the WM performance in the WM-only
session and dark grey indicates the WM performance in the
WM + pursuit session. (A) accuracy, (B) reaction times. Error
bars represent standard error and asterisks indicate significance
at p &#x3C;  0.05. </p>
					</caption>
					<graphic id="graph02" xlink:href="jemr-10-03-f-figure-02.png"/>
				</fig>
      <p>We also compared the pursuit performance in the
WM + pursuit session and the pursuit-only session to
investigate whether adding secondary WM task would
affect the pursuit performance. We found a significantly
lower peak open loop gain (F(1,15)=14.39, p=0.002) in
the WM + pursuit session (0.77 &#xB1; 0.05) compared with
pursuit-only session (0.89 &#xB1; 0.05). In addition, the
steadystate velocity gain was also lower in WM + pursuit
session (0.92 &#xB1; 0.024) than in the pursuit-only session
(0.98&#xB1;0.014) (F(1,15)=10.57, p=0.005). These results
indicated the addition of the secondary WM task harmed
the pursuit performance.</p>
      <p>Combining these results, we see that the WM and
pursuit interfere with each other. However, it is still
unclear whether it is general for secondary task or specific
to the eye movement type. To check this, we analyzed the
data from the WM + pursuit session in details.</p>
      
	  
	  
	  <p><xref ref-type="fig" rid="fig03">Figure 3</xref> shows the performance of working memory
in the WM + pursuit session, which was assessed using a
two-way repeated-measure ANOVA for load (load 2 vs.
load 4) and consistency (consistent vs. inconsistent).
Consistent with previous findings, the accuracy was
decreased with higher load (F(1,15)=92.53, p=0.000) and
the consistent condition revealed higher accuracy than the
inconsistent condition (F(1,15)=4.73, p=0.046). No
interaction between the load and consistency. Similarly, the
reaction times increased with higher load (F(1,15)=14.50,
p=0.002) and the consistent condition showed shorter
reaction times than the inconsistent condition
(F(1,15)=5.23, p=0.037). Further post hoc t-tests,
Bonferroni corrected for multiple comparisons, showed longer
reaction times in the inconsistent condition (881.6 &#xB1; 48.1
ms) than in the consistent condition (832.3 &#xB1; 45.6 ms)
(Bonferroni adjusted t(15) = 3.15, p = 0.007) with load 2.
In this comparison, the significance level was adjusted to
0.0083 (0.05/6 = 0.0083) due to 6 possible comparisons
across the 4 conditions (4*3/2 = 6).</p>
     <fig id="fig03" fig-type="figure" position="float">
					<label>Figure 3</label>
					<caption>
						<p>The performance of color WM in the WM + pursuit
session. (A) accuracy. (B) reaction time. Error bars represent
standard error. Asterisks indicate significance at p &#x3C;  0.05. </p>
					</caption>
					<graphic id="graph03" xlink:href="jemr-10-03-f-figure-03.png"/>
				</fig>

	 <p>Combining the accuracy and reaction time results, we
found pursuing towards the locations where the WM
stimuli were presented produced better WM performance
than pursuing away from those during the retention
period. In addition, we computed the mean horizontal eye
positions in a 200 ms time window since the test display
onset to see whether eyes returned to the central fixation
cross. A two-way repeated-measures ANOVA on load
(load 2 vs. load 4) and consistency (consistent vs.
inconsistent) showed a significant effect of consistency
(F(1,15)=5347.64, P=0.000) and interaction between load
and consistency (F(1,15)=14.46, P=0.002). Further
comparison showed that the eyes deviated more from the
fixation cross with load 2 (9.857 degree) compared with
load 4 (9.510 degree) (t(15) = 2.59, p = 0.021). These
data showed that the eyes posited around the positions
where pursuit ended and had not returned to the fixation
cross yet when the test display appeared, resulting in
bigger retinal eccentricity in the inconsistent condition.
Interestingly, the retinal eccentricity was smaller with
load 4 than with load 2, indicating that memorizing more
colors urged eye to return to the central fixation.</p>
      
	  
	 
      <p>In addition, to check the effect of the WM on the
pursuit, we analyzed the open-loop gain and steady-state
gain using a two-way repeated-measures ANOVA using
load (load 2 vs. load 4) and consistency (consistent vs.
inconsistent) as factors respectively <xref ref-type="fig" rid="fig04">Figure 4</xref>. The
ANOVA revealed lower open-loop gain (F(1,15)=29.50,
p=0.000) and steady-state gain (F(1,15)=10.08, p=0.006)
with higher load. Moreover, the steady-state gain was
higher in the inconsistent condition (F(1,15)=8.30,
p=0.011) and there was a marginally significant
interaction between the load and consistency (F(1,15)=3.85,
p=0.069). Further pairwise comparison using 0.0083
(0.05/6 = 0.0083) as the significance level due to 6
possible comparisons across the 4 conditions (4*3/2 = 6)
showed mean steady state gain in the inconsistent
condition was higher than that in the consistent condition with
higher WM load (Bonferroni adjusted t(15) = 3.28,
p=0.008). Additionally, we also found higher saccade
frequency with higher load (F(1,15)=9.31, p=0.008),
indicating the worse pursuit performance with higher
load. Overall, these results showed that the pursuit 
performance was further impaired by higher load and the
steady-state performance was even influenced by the
consistency between the WM and the pursuit.</p>
<fig id="fig04" fig-type="figure" position="float">
					<label>Figure 4</label>
					<caption>
						<p>The pursuit performance in the WM + pursuit session. (A) Mean eye velocity trace in all conditions from target
onset for a representative subject. The two horizontal line means the target velocity. (B) Peak open loop acceleration for all
subjects averaged in the open loop period. (C) Eye velocity gain for all subjects averaged in the steady state. (D) Saccade frequency
in the retention interval. Error bars represent standard error. Asterisks indicate significance at p &#x3C;  0.05.</p>
					</caption>
					<graphic id="graph04" xlink:href="jemr-10-03-f-figure-04.png"/>
				</fig>


      <p>In order to check whether the change of squares&#x2019;
colors in the uncued VF affected the WM performance, we
grouped the trials in two types in each load condition for
the data from the WM only session. One type included
trials with the color change (change) and the other type
included trials without color change (same) in the uncued
VF. Since the color changes in the cued and uncued VF
were independent each other and all trial type had equal
opportunities, we would not expect an effect of the trial
type. We assessed the WM performance using the
repeated-measures ANOVA for WM load (load 2 vs. load 4)
and trial type (same vs. change). There was only a
significant effect of load for accuracy (F(1,15)=300.95,
p=0.000) and no effect of the trial type was found,
indicating that the color change in the uncued VF did not
affect he WM performances. Therefore, we suggested
that the subjects followed the instruction.</p>
    </sec>
	
	 <sec id="s4">
      <title>Discussion</title>
      <p>In the current study, we showed that the color WM
and the smooth pursuit eye movements interfered with
each other. More interestingly, pursuing towards the cued
visual field resulted in enhanced color WM performance
compared with pursuing away from it. In turn, the higher
load of WM impaired the pursuit performance more than
the lower load of WM.</p>
      <p>The color WM performance was impaired by adding
the pursuit task during the retention period and the
pursuit performance was also impaired by adding the color
WM task, demonstrating that the color WM and smooth
pursuit interfere each other and further suggesting smooth
pursuit share common resources. We think that common
attentional resources shared by the color WM and SPEM
might be of central, amodal origin, which might point to
the central executive component in Baddeley&#x2019;s model
(2000). This also agrees with the resource model of
working memory which propose that a limited resource is
distributed flexibly across all representations which are
maintained in memory
        <xref ref-type="bibr" rid="b27">(Ma, Husain &amp; Bays, 2014)</xref>
        .
Consistently, higher WM load impaired the pursuit
performance more as shown by the lower open-loop gain and
steady state gain, and higher saccade frequency in the
load 4 condition.</p>
      <p>In turn, greater impairment of the color WM
performance which was shown by lower accuracy and longer
reaction time, was observed in the inconsistent condition
where the pursuit during the retention period was away
from the location of the WM stimuli, showing that the
direction of smooth pursuit plays a role in our WM task.
In the current study, the fixation cross moved towards or
away from the cued VF from the display center.
Therefore, in the trials where the cross pursued towards the
cued VF, the smooth pursuit target moved within the
cued VF during the whole retention period and vice
versa. Studies agreed that attention is narrowly distributed
around the pursuit target, while they disagree about the
symmetry of the attention distribution during smooth
pursuit
        <xref ref-type="bibr" rid="b18 b20 b26 b37 b38 b45 b46">(Kanai, van der Geest, &amp; Frens, 2003; Khan,
Lefe`vre, Heinen, &amp; Blohm, 2010; Seya &amp; Mori, 2012;
Smeets &amp; Bekkering, 2000; van Donkelaar &amp; Drew,
2002; Lovejoy et al., 2009; Watamaniuk &amp; Heinen,
2015)</xref>
        . Hence, we propose that more attention could be
distributed in the cued VF during the retention period in
the consistent condition and more attention benefited the
color WM. The results showed that shifting attention
smoothly to the locations where the memory target was
presented would help the color WM compared to when
shifting attention away from it. These results mimic
attention-based rehearsal hypothesis
        <xref ref-type="bibr" rid="b3">(Awh &amp; Jonides,
2001)</xref>
        . This hypothesis proposes the rehearsal of stored
spatial information is accomplished by shifts of spatial
selective attention to memorized locations. Therefore, our
finding further extends the hypothesis to the relationship
between spatial attention and non-spatial WM and further
suggest that spatial attention plays a functional role in
maintaining non-spatial information. However, our
results could not exclude the possible effect caused by the
closer eye position to the WM target in the consistent
condition at the onset of the test display.</p>
      <p>At the same time, the pursuit performance was better
in the inconsistent condition than in the consistent
condition during the steady-state, especially when the WM
load was higher. Since spatial attention plays an
important role in maintaining location information
        <xref ref-type="bibr" rid="b3">(Awh &amp;
Jonides, 2001)</xref>
        and attention is allocated around the
pursuit target, a conflict or competition of attention resources
might occur in the inconsistent condition, especially
when the demand for attentional resources is intensified.
This imitates the anti-saccade task, which requires
subjects to suppress a reflexive saccade towards a visual
stimulus and perform a voluntary saccade away from the
target
        <xref ref-type="bibr" rid="b11 b13">(Cutsuridis et al. 2007; Everling &amp; Fischer 1998)</xref>
        .
Therefore, the pursuit in the inconsistent condition was
more difficult than that in the consistent condition and
more cognitive control is needed for the pursuit in the
inconsistent condition. This is in line with the previous
finding that eye-target synchronization improved under
higher cognitive load (five-words) for normal subjects
        <xref ref-type="bibr" rid="b8">(Contreras et al., 2011)</xref>
        .</p>
      <p>Taken together, our results are in line with the finding
from
        <xref ref-type="bibr" rid="b28">Makovski and Jiang (2009)</xref>
        and support that the
visual WM and smooth pursuit share common attentional
resources. Due to the presentation of the colored squares
on the display, it is still possible that the locations of
squares were encoded and memorized automatically.
However, we tried to reduce this possibility by fixing the
possible locations of the squares in each condition and
forbidding exchanging colors between squares when
comparing the colors of the target and test stimuli. Such a
design reduced possible effect of stimuli location, so we
suggest that our results can be interpreted as the
relationship between the color WM and smooth pursuit. Many
studies have shown persistent neural activities during the
retention period of WM in the prefrontal areas
        <xref ref-type="bibr" rid="b14">(Funahashi
et al., 1993)</xref>
        , frontal eye fields
        <xref ref-type="bibr" rid="b10 b42">(Curtis et al., 2004; Tark &amp;
Curtis, 2009)</xref>
        and posterior parietal cortex <xref ref-type="bibr" rid="b36">(Schluppeck et
al., 2006)</xref>. Since smooth pursuit-related brains areas
mainly involve fronto-parietal network, such as the
frontal eye field, supplementary eye fields and posterior
parietal cortex, there are many overlaps in the brain areas
related to the WM and smooth pursuit. Similarly, we
supposed that there might be a competition for the shared
neural resources of fronto-parietal network, resulting in
competition between the color WM and pursuit tasks.</p>
      <p>In sum, the current study found mutual interference
between the color WM task and smooth pursuit eye
movements. Furthermore, the pursuit direction plays a
role in the color WM that the color WM benefited when
pursuing towards the locations where the WM stimuli
were presented. We propose that it is because more
attentional resources are directed to the locations of the WM
stimuli during the retention period by the help of the
smooth pursuit eye movements.</p>
      <sec id="s4a" sec-type="COI-statement">
        <title>Ethics and Conflict of Interest</title>
        <p>The authors declare that the contents of the article are
in agreement with the ethics described in<ext-link ext-link-type="uri" xlink:href="http://biblio.unibe.ch/portale/elibrary/BOP/jemr/ethics.html" xlink:show="new">http://biblio.unibe.ch/portale/elibrary/BOP/jemr/ethics.html</ext-link> and that there is no conflict of interest regarding the
publication of this paper.</p>
      </sec>
      <sec id="s4b">
        <title>Acknowledgements</title>
        <p>This work was supported by grants from Natural
Science Foundation of China (Nos 61673087, 61473062 and
61203363), and the Fundamental Research Funds for the
Central Universities.</p>
        <p>S.Y. conducted the experiment, analyzed data and
wrote the manuscript. Z.J. designed the experiment and
revised the manuscript. C.F. prepared figures and Q.Z.
proofed article. L.L. designed the experiment. All authors
reviewed the article.</p>
      </sec>
    </sec>
  
    </body>
  
  
  
  
  
  <back>
  
  
  
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