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Improvement in Visual Search with Practice: Mapping Learning-Related Changes in Neurocognitive Stages of Processing

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Improvement in Visual Search with Practice: Mapping Learning-Related Changes in Neurocognitive Stages of Processing The Journal of Neuroscience, April 1, 2015 • 35(13):5351–5359 • 5351 Behavioral/Cognitive Improvement in Visual Search with Practice: Mapping Learning-Related Changes in Neurocognitive Stages of Processing Kait Clark,1,3 L. Gregory Appelbaum,1,4 Berry van den Berg,1,5 Stephen R. Mitroff,1,2 and Marty G. Woldorff1,2,4 1Center for Cognitive Neuroscience and 2Department of Psychology and Neuroscience, Duke University, Durham, North Carolina 27708, 3School of Psychology, Cardiff University, Cardiff CF10 3AT, United Kingdom, 4Department of Psychiatry, Duke University Medical Center, Durham, North Carolina 27708, and 5BCN Neuroimaging Center, University of Groningen, 9700 AB Groningen, The Netherlands Practice can improve performance on visual search tasks; the neural mechanisms underlying such improvements, however, are not clear. Response time typically shortens with practice, but which components of the stimulus–response processing chain facilitate this behav- ioral change? Improved search performance could result from enhancements in various cognitive processing stages, including (1) sensory processing, (2) attentional allocation, (3) target discrimination, (4) motor-response preparation, and/or (5) response execution. We measured event-related potentials (ERPs) as human participants completed a five-day visual-search protocol in which they reported the orientation of a color popout target within an array of ellipses. We assessed changes in behavioral performance and in ERP compo- nents associated with various stages of processing. After practice, response time decreased in all participants (while accuracy remained consistent), and electrophysiological measures revealed modulation of several ERP components. First, amplitudes of the early sensory- evoked N1 component at 150 ms increased bilaterally, indicating enhanced visual sensory processing of the array. Second, the negative- polarity posterior–contralateral component (N2pc, 170–250 ms) was earlier and larger, demonstrating enhanced attentional orienting. Third, the amplitude of the sustained posterior contralateral negativity component (SPCN, 300–400 ms) decreased, indicating facilitated target discrimination. Finally, faster motor-response preparation and execution were observed after practice, as indicated by latency changes in both the stimulus-locked and response-locked lateralized readiness potentials (LRPs). These electrophysiological results delineate the functional plasticity in key mechanisms underlying visual search with high temporal resolution and illustrate how practice influences various cognitive and neural processing stages leading to enhanced behavioral performance. Key words: attention; EEG; learning; LRP; N2pc; visual search Introduction view, see Eckstein, 2011; Nakayama and Martini, 2011). These Visual search, the process of detecting target items among dis- cognitive faculties are supported by various underlying neural tractors, is a vital cognitive ability central to many everyday hu- mechanisms ranging from low-level feature analyses to higher-level, man activities, as well as to societally critical job tasks such as goal-driven decision processes (Treisman and Gelade, 1980;Duncan detecting abnormalities in radiological images and screening air- and Humphreys, 1989; Corbetta and Shulman, 2002). port luggage for contraband (for review, see Clark et al., 2012; Prior research has established that visual search can be improved Wetter, 2013). Successful search requires the execution of a cas- through experience or practice (Sireteanu and Rettenbach, 1995; cade of fundamental cognitive processes, including sensory anal- Sigman and Gilbert, 2000). Given the numerous neurocognitive ysis of the scene, orienting of visual attention, working memory, stages involved in detecting, assessing, and responding to search target discrimination, and decision/response processes (for a re- stimuli, questions remain as to which processes are enhanced and in what relative combination. Several recent visual search studies have reported amplitude changes in certain scalp-recorded event-related Received March 21, 2014; revised Dec. 11, 2014; accepted Jan. 22, 2015. potential (ERP) components after practice on complex conjunction Author contributions: K.C., L.G.A., S.R.M., and M.G.W. designed research; K.C., L.G.A., and M.G.W. performed research; K.C., L.G.A., and B.v.d.B. analyzed data; K.C., L.G.A., S.R.M., and M.G.W. wrote the paper. search tasks (Hamame et al., 2011; An et al., 2012); however, the ThisworkwassupportedbyU.S.NIHGrantR01-MH060415toM.G.W,withsomesupportfromU.K.ESRC/ORAϩ learning-related changes underlying training-induced behavioral Grant ES/M00001X/1. improvement in the rapid, tightly timed, parallel processing in- The authors declare no competing financial interests. volved in feature-popout search tasks are unclear. This article is freely available online through the J Neurosci Author Open Choice option. Correspondence should be addressed to Marty G. Woldorff, Center for Cognitive Neuroscience, Duke University, Here, we investigated changes across the entire stimulus– Box 90999, Durham, NC 27708. E-mail: [email protected]. response processing cascade that underlies popout visual search DOI:10.1523/JNEUROSCI.1152-14.2015 learning by leveraging the high temporal resolution of ERPs elic- Copyright © 2015 Clark et al. ited while searching visual arrays containing rapidly processed This is an Open Access article distributed under the terms of the Creative Commons Attribution License CreativeCommonsAttribution4.0International,whichpermitsunrestricteduse,distributionandreproductioninany feature-popout targets. Participants completed a five-day behav- medium provided that the original work is properly attributed. ioral practice protocol (with electrophysiological activity re- 5352 • J. Neurosci., April 1, 2015 • 35(13):5351–5359 Clark et al. • Visual Search Practice Figure 1. Hypothetical model indicating potential changes in behavior and ERP components in a visual search task after practice. A, Response time (RT) is expected to decrease after practice. B, Horizontal arrows indicate potential latency shifts in the N1, N2pc, and LRP components. Vertical arrows indicate potential amplitude changes in the P1/N1, N2pc, and SPCN components. corded on days 1 and 5) to explore plasticity in the neural mechanisms underlying the expected practice-induced reduction in behavioral response time (Fig. 1A). We assessed changes in four hallmark ERP components that reflect the cascade of cognitive processing stages from stimulus to response (Fig. 1B): (1) the posterior visual N1, a negative-polarity wave (latency ϳ150 ms) that reflects early sensory-evoked pro- cessing (Mangun and Hillyard, 1991); (2) the negative-polarity posterior–contralateral N2pc component (latency ϳ225 ms) as- sociated with the shift of attention to a lateralized stimulus loca- tion (Luck and Hillyard, 1994a); (3) the sustained posterior– contralateral negativity (SPCN) component (latency 300–450 ms) or contralateral delay activity (CDA) that has been linked to maintenance and manipulation of information in visual working memory (Jolicoeur et al., 2008; Ikkai et al., 2010) and/or to cog- nitive processing demands for target discrimination (Emrich et al., 2009; Luria and Vogel, 2011); and (4) the motor-related lat- eralized readiness potential (LRP) that reflects the initiation of a motor response (Coles, 1988). Figure 2. Sample stimulus display. The blue ellipses were distractors, the green ellipse was By comparing the neural activity associated with these cogni- the relevant color popout target, and the red ellipse was the irrelevant color popout nontarget. tive processes before and after the practice regimen, we aimed to Participants responded as to the orientation of the green target ellipse. In this example, a elucidate neural plasticity underlying the expected improve- participant would respond by pressing the button corresponding to “horizontal.” ments in visual search efficiency. Specifically, we assessed changes in the amplitude and/or latency of these ERP components to Search paradigm reveal how enhancements in sensory processing, attentional ori- Stimuli were programmed and presented using the Presentation software enting, target discrimination, motor initiation, and/or motor ex- suite (Neurobehavioral Systems). During each of the five experimental ecution contribute to improvement in visual search with practice. sessions, participants completed a series of 14 blocks, each consisting of 140 trials and lasting ϳ4 min. Thus, each experimental session com- Materials and Methods prised 1960 trials and lasted ϳ56 min. Participants were seated without Participants head restraint ϳ57 cm from the viewing monitor. A white fixation cross Nineteen healthy individuals with normal or corrected-to-normal visual was presented at the center of the screen on a gray background and acuity and normal color vision were recruited and provided informed remained in place for the duration of each experimental block. Each trial consent. All procedures were approved by the Duke University Medical consisted of a briefly presented (50 ms) circular array of 48 colored Center Institutional Review Board. All individuals participated in a five- ellipses of which 46 were blue, 1 was red, and 1 was green (Fig. 2), with day visual search practice protocol for approximately 1 hour per day, each stimulus subtending a visual angle of 1.36 ϫ 0.91°. Thus, on each over 5 consecutive days, beginning on a Monday and ending on the trial,
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