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Stimulus–response bindings in priming

Identifieur interne : 000051 ( Pmc/Checkpoint ); précédent : 000050; suivant : 000052

Stimulus–response bindings in priming

Auteurs : Richard N. Henson [Royaume-Uni] ; Doris Eckstein [Suisse] ; Florian Waszak [France] ; Christian Frings [Allemagne] ; Aidan J. Horner [Royaume-Uni]

Source :

RBID : PMC:4074350

Abstract

Highlights

S–R bindings are more flexible and pervasive than previously thought.

S–R bindings can simultaneously encode multiple stimulus and response representations.

S–R bindings can be encoded or retrieved in the absence of attention or awareness.

S–R bindings complicate interpretations of priming, but are interesting in their own right.

S–R bindings enable rapid yet context-dependent behaviors.


Url:
DOI: 10.1016/j.tics.2014.03.004
PubMed: 24768034
PubMed Central: 4074350


Affiliations:


Links toward previous steps (curation, corpus...)


Links to Exploration step

PMC:4074350

Le document en format XML

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<p>S–R bindings can simultaneously encode multiple stimulus and response representations.</p>
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<p>S–R bindings can be encoded or retrieved in the absence of attention or awareness.</p>
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<p>S–R bindings complicate interpretations of priming, but are interesting in their own right.</p>
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<p>S–R bindings enable rapid yet context-dependent behaviors.</p>
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</TEI>
<pmc article-type="review-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Trends Cogn Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Trends Cogn. Sci. (Regul. Ed.)</journal-id>
<journal-title-group>
<journal-title>Trends in Cognitive Sciences</journal-title>
</journal-title-group>
<issn pub-type="ppub">1364-6613</issn>
<issn pub-type="epub">1879-307X</issn>
<publisher>
<publisher-name>Elsevier Science</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">24768034</article-id>
<article-id pub-id-type="pmc">4074350</article-id>
<article-id pub-id-type="publisher-id">S1364-6613(14)00076-X</article-id>
<article-id pub-id-type="doi">10.1016/j.tics.2014.03.004</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Review</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Stimulus–response bindings in priming</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<name>
<surname>Henson</surname>
<given-names>Richard N.</given-names>
</name>
<email>rik.henson@mrc-cbu.cam.ac.uk</email>
<xref rid="aff0005" ref-type="aff">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Eckstein</surname>
<given-names>Doris</given-names>
</name>
<xref rid="aff0010" ref-type="aff">2</xref>
<xref rid="aff0015" ref-type="aff">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Waszak</surname>
<given-names>Florian</given-names>
</name>
<xref rid="aff0020" ref-type="aff">4</xref>
<xref rid="aff0025" ref-type="aff">5</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Frings</surname>
<given-names>Christian</given-names>
</name>
<xref rid="aff0030" ref-type="aff">6</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Horner</surname>
<given-names>Aidan J.</given-names>
</name>
<xref rid="aff0035" ref-type="aff">7</xref>
<xref rid="aff0040" ref-type="aff">8</xref>
</contrib>
</contrib-group>
<aff id="aff0005">
<label>1</label>
MRC Cognition and Brain Sciences Unit, Cambridge, UK</aff>
<aff id="aff0010">
<label>2</label>
Institut für Psychologie, Universität Bern, Bern, Switzerland</aff>
<aff id="aff0015">
<label>3</label>
Center for Cognition, Learning, and Memory, Universität Bern, Bern, Switzerland</aff>
<aff id="aff0020">
<label>4</label>
Institut Neurosciences Cognition, Université Paris Descartes, Paris, France</aff>
<aff id="aff0025">
<label>5</label>
CNRS Laboratoire Psychologie de la Perception UMR 8242, Université Paris Descartes, Paris, France</aff>
<aff id="aff0030">
<label>6</label>
Allgemeine Psychologie und Methodenlehre, Universtät Trier, Trier, Germany</aff>
<aff id="aff0035">
<label>7</label>
Institute of Cognitive Neuroscience, University College London, London, UK</aff>
<aff id="aff0040">
<label>8</label>
Institute of Neurology, University College London, London, UK</aff>
<pub-date pub-type="pmc-release">
<day>1</day>
<month>7</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub">
<month>7</month>
<year>2014</year>
</pub-date>
<volume>18</volume>
<issue>7</issue>
<fpage>376</fpage>
<lpage>384</lpage>
<permissions>
<copyright-statement>© 2014 The Authors</copyright-statement>
<copyright-year>2014</copyright-year>
<license license-type="CC BY" xlink:href="http://creativecommons.org/licenses/by/3.0/">
<license-p>This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/3.0/).</license-p>
</license>
</permissions>
<abstract abstract-type="author-highlights">
<title>Highlights</title>
<p>
<list list-type="simple">
<list-item id="lsti0005">
<label></label>
<p>S–R bindings are more flexible and pervasive than previously thought.</p>
</list-item>
<list-item id="lsti0010">
<label></label>
<p>S–R bindings can simultaneously encode multiple stimulus and response representations.</p>
</list-item>
<list-item id="lsti0015">
<label></label>
<p>S–R bindings can be encoded or retrieved in the absence of attention or awareness.</p>
</list-item>
<list-item id="lsti0020">
<label></label>
<p>S–R bindings complicate interpretations of priming, but are interesting in their own right.</p>
</list-item>
<list-item id="lsti0025">
<label></label>
<p>S–R bindings enable rapid yet context-dependent behaviors.</p>
</list-item>
</list>
</p>
</abstract>
<abstract>
<p>People can rapidly form arbitrary associations between stimuli and the responses they make in the presence of those stimuli. Such stimulus–response (S–R) bindings, when retrieved, affect the way that people respond to the same, or related, stimuli. Only recently, however, has the flexibility and ubiquity of these S–R bindings been appreciated, particularly in the context of priming paradigms. This is important for the many cognitive theories that appeal to evidence from priming. It is also important for the control of action generally. An S–R binding is more than a gradually learned association between a specific stimulus and a specific response; instead, it captures the full, context-dependent behavioral potential of a stimulus.</p>
</abstract>
<kwd-group>
<title>Keywords</title>
<kwd>S–R bindings</kwd>
<kwd>repetition suppression</kwd>
<kwd>automaticity</kwd>
<kwd>masked priming</kwd>
<kwd>subliminal priming</kwd>
<kwd>negative priming</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="fig0005">
<label>Figure 1</label>
<caption>
<p>Schematic of component processes, stimulus–response (S–R) bindings, and priming paradigms.
<bold>(A)</bold>
When someone is asked to make a decision about a stimulus (e.g., whether the object depicted by an image is living or nonliving), several component processes are required to, for example, identify perceptually the object (here, a lion) and retrieve conceptual information about it (that a lion is a living entity) (top row). When that stimulus is presented a second time, the reaction time (RT) to make the same judgment is normally faster, a phenomenon called priming. This could reflect facilitation of one or more of the component processes engaged on initial presentation (second row) or it could reflect retrieval of an S–R binding that encodes the stimulus and response made on the initial presentation, without needing to re-engage the original component processes (third row).
<bold>(B)</bold>
The three main types of priming paradigm considered here are repetition priming (top row), negative priming (middle row), and masked priming (bottom row). The initial presentation is shown on the left and the repeat presentation on the right. In the case of negative priming, the red square indicates the target stimulus to which participants attend to determine their response (other concurrent stimuli are distractors). In the masked priming case, the prime is often presented for less than 50 ms and followed by a backward mask (illustrated by a square of pixel noise here) to render it subliminal. The broken lines indicate potential encoding or retrieval of an S–R binding.</p>
</caption>
<graphic xlink:href="gr1"></graphic>
</fig>
<fig id="fig0010">
<label>Figure 2</label>
<caption>
<p>Possible stimulus–response (S–R) binding. Schematic of a possible structured S–R binding formed by giving a response to a picture of a lion during a binary ‘bigger than shoebox?’ categorization task, where red lines indicate bindings. Stimulus representations include a visual image of the picture and a more abstract representation of the identity of that stimulus, such that if the word ‘lion’ is later presented, it can also cue responses via the bindings between the identity representation and response representations. Response representations include a specific motor action (e.g., right index finger depression), a binary decision (e.g., ‘yes’) and a particular classification (e.g., ‘bigger’ in the size task). This means that retrieval of an action or decision can influence responses even if the task is changed; for example, to an ‘is the object living?’ categorization instead (as shown). Similarly, retrieval of a decision can influence responses even if the effector (action) is changed and retrieval of a classification can influence responses even if the task (and hence decision and action) is reversed (e.g., to a ‘smaller than shoebox?’ task). Retrieval of the S–R binding may also be mediated by the spatial/temporal context (e.g., laboratory setting).</p>
</caption>
<graphic xlink:href="gr2"></graphic>
</fig>
<fig id="fig0015">
<label>Figure 3</label>
<caption>
<p>Neural correlates of stimulus–response (S–R) retrieval.
<bold>(A,B)</bold>
Data from the functional MRI (fMRI) study of Dobbins
<italic>et al.</italic>
<xref rid="bib0315" ref-type="bibr">[63]</xref>
in which simply reversing the task in a repetition priming paradigm reduced repetition suppression (RS). In the start phase, participants judged whether visual objects were bigger than a shoebox; in the switch phase, the same objects (together with new, unprimed objects) were judged as to whether they were smaller than a shoebox (in the return phase, the original ‘bigger’ task was reinstated). The red patches in the three views of a canonical brain in (A) indicate regions showing smaller responses to primed than unprimed trials in the start phase (i.e., RS). The plots in (B) show the average fMRI evoked response to unprimed (dark blue) and primed (light blue) trials from two representative such regions: the prefrontal cortex (PFC) and the ventrotemporal cortex (fusiform). Note that RS in the fusiform is abolished when the task is reversed. Dobbins
<italic>et al.</italic>
suggested that the RS in the start phase reflected bypassing of component processes when S–R bindings are retrieved, whereas the lack of RS in the switch phase arises when S–R bindings are no longer used. Reproduced, with permission, from
<xref rid="bib0315" ref-type="bibr">[63]</xref>
.
<bold>(C,D)</bold>
Data from the event-related potential (ERP) study of Horner and Henson
<xref rid="bib0400" ref-type="bibr">[80]</xref>
. Participants performed the same size-judgment task as in Dobbins
<italic>et al.</italic>
, except that the referent object (e.g., a shoebox) was switched between prime and probe to render the previous response congruent or incongruent. (C) A time window (grey box) within a stimulus-locked ERP over parietal electrodes during which an effect of stimulus repetition was seen that was not modulated by whether the response was repeated or reversed between presentations (at least until later). (D) An effect over frontal electrodes showed a response congruency effect for primed (repeated) stimuli, but for not unprimed (novel) stimuli, a few hundred milliseconds before a key was pressed (i.e., response-locked). Whereas the stimulus-locked effect was hypothesized to reflect the facilitation of (perceptual) component processes, the response-locked effect was hypothesized to reflect decision processes that resolve the conflict when responses retrieved from S–R bindings and responses generated by component processes are incongruent. Reproduced, with permission, from
<xref rid="bib0400" ref-type="bibr">[80]</xref>
.</p>
</caption>
<graphic xlink:href="gr3"></graphic>
</fig>
<boxed-text id="tb0005">
<label>Box 1</label>
<caption>
<title>Major types of priming</title>
</caption>
<p>Priming refers to a change in accuracy, bias, or reaction time to respond to a stimulus (‘probe’) owing to prior presentation of the same or a similar stimulus (‘prime’). It is indexed as the difference between the response to the prime and probe or between the probe and a comparable stimulus not presented before (‘unprimed’). There are at least three main priming paradigms, which differ in whether a response is made to: (i) the prime; and/or (ii) the probe (see
<xref rid="fig0005" ref-type="fig">Figure 1</xref>
B in main text).</p>
<p>In repetition priming, a response is made to both prime and probe. The prime and probe typically occur in separate trials separated by multiple intervening trials (so that priming does not simply owe to repetition of the same response across successive trials; that is, ‘response priming’). Note that the stimulus may not be repeated in exactly the same physical form (e.g., it may switch from a written to a spoken word across trials).</p>
<p>In negative priming, the prime (and sometimes the probe) is a distractor; that is, it is not the focus of attention, such that the response is generated instead by a different, concurrent stimulus. Responses are typically slowed when the prime is then presented as a probe in a subsequent trial (although note that priming is not always ‘negative’ in the sense of a slowing; positive priming can occur if the response previously paired with the prime is congruent with that required to the probe).</p>
<p>In masked priming, the prime is masked to render it subliminal, such that no response can be made to it. The subsequent supraliminal probe typically occurs within a few hundred milliseconds (i.e., within the same trial). The S–R binding that is potentially retrieved by the masked prime then usually comes from previous presentations of the same stimulus as a probe in other trials.</p>
<p>These paradigms differ in other ways too. For example, repetition priming can survive lags of many intervening trials and sometimes last days, whereas negative priming typically occurs only across successive trials and masked priming rarely lasts beyond one trial. There are also other priming paradigms (e.g., semantic/affective priming, where prime and probe are different stimuli but semantically or affectively related), but here we focus on paradigms in which S–R bindings have been shown to play a dominant role, and these normally involve repeating a stimulus to cue retrieval of an S–R binding (although see text about possible F–R bindings).</p>
</boxed-text>
<boxed-text id="tb0010">
<label>Box 2</label>
<caption>
<title>S–R theories</title>
</caption>
<p>There are many theories relating to S–R bindings; we focus on one example pertinent to each of the three priming paradigms considered here (
<xref rid="tb0005" ref-type="boxed-text">Box 1</xref>
).</p>
<p>Logan proposed an ‘instance theory’
<xref rid="bib0320" ref-type="bibr">[64]</xref>
of automaticity that has been mainly applied to repetition priming. Responses are determined by a race between an algorithmic route (comprising computations used to produce a response the first time a stimulus is encountered) and retrieval of any relevant S–R bindings (with a separate such ‘instance’ stored each time a response is given to a stimulus). Assuming that all S–R bindings race independently, RTs will decrease with the number of instances according to a power law, with the mean and standard deviation having the same exponent. A later version of the theory
<xref rid="bib0370" ref-type="bibr">[74]</xref>
included two additional decision rules (a counter and a random-walk model) that prioritize response accuracy at the cost of increased RTs in conflict situations. With this extension, instance theory can also potentially explain negative priming.</p>
<p>Hommel
<xref rid="bib0155" ref-type="bibr">[31]</xref>
hypothesized the existence of ‘episodic records’. These encode features of stimuli and responses, with each record binding only two features (which can be from different stimuli), although the same feature can occur in multiple records. Hommel's theory was developed primarily to explain ‘carry-over’ costs from one trial to the next (such as negative priming), rather than longer-lived facilitatory effects seen in repetition priming paradigms.</p>
<p>Kunde
<italic>et al.</italic>
<xref rid="bib0375" ref-type="bibr">[75]</xref>
proposed an ‘action trigger’ theory (see also
<xref rid="bib0380" ref-type="bibr">[76]</xref>
), which is most often applied to masked priming. The basic idea is that repeated pairings of a stimulus and response establish a trigger that releases an action when a related stimulus reappears. The generalization to related stimuli comes from being able to specify the trigger conditions in broad terms. For example, evidence that the masked digit ‘3’ can prime a relative size judgment to a subsequent probe ‘4’, even if the 3 was not presented previously in the experiment
<xref rid="bib0300" ref-type="bibr">[60]</xref>
, can be explained by a generic trigger of the sort ‘small numbers should produce a “no” response’.</p>
<p>Although these S–R theories have proved helpful, each needs further development to explain the precise role of attention and awareness during encoding and retrieval of S–R bindings (see text) and their interactions with other component processes. Moreover, few if any theories specify neural mechanisms that can be compared with recent brain data (
<xref rid="tb0015" ref-type="boxed-text">Box 3</xref>
).</p>
</boxed-text>
<boxed-text id="tb0015">
<label>Box 3</label>
<caption>
<title>S–R bindings in the brain</title>
</caption>
<p>Another reason for the resurgence of interest in S–R bindings concerns recent neuroimaging and neuropsychological data. In particular, the phenomenon of ‘repetition suppression’ has been assumed to reflect the facilitation of component processes and therefore used to map neural representations in different brain regions
<xref rid="bib0385 bib0390" ref-type="bibr">[77,78]</xref>
. An influential functional MRI (fMRI) study by Dobbins
<italic>et al.</italic>
<xref rid="bib0315" ref-type="bibr">[63]</xref>
, however, suggested that repetition suppression in ventrotemporal regions (associated with visual object perception) reflects instead the bypassing of such processes owing to retrieval of S–R bindings (see
<xref rid="fig0015" ref-type="fig">Figure 3</xref>
A in main text). Although later studies suggested that S–R bindings cannot explain all repetition suppression in perceptual regions, retrieval of S–R bindings clearly has important effects on neuroimaging data
<xref rid="bib0075 bib0395" ref-type="bibr">[15,79]</xref>
. Recent work has focused on relating the effects of response congruency in prefrontal cortex to the integration of: (i) responses retrieved from S–R bindings; and (ii) responses generated from component processes
<xref rid="bib0075 bib0400" ref-type="bibr">[15,80]</xref>
.</p>
<p>Effects of response congruency have been found in response-locked event-related potentials (ERPs) over frontal electrodes a few hundred milliseconds before the response occurs
<xref rid="bib0075 bib0400" ref-type="bibr">[15,80]</xref>
(see
<xref rid="fig0015" ref-type="fig">Figure 3</xref>
D in main text). ERPs locked to stimulus onset, by contrast, appear less affected by response congruency, suggesting that stimulus repetition effects on these ERPs may reflect facilitation of component processes. Stimulus repetition also modulates 5–15-Hz power in ventrotemporal regions as measured by magnetoencephalography (MEG)
<xref rid="bib0405" ref-type="bibr">[81]</xref>
and increases the synchrony of this oscillatory activity between prefrontal and ventrotemporal regions
<xref rid="bib0410" ref-type="bibr">[82]</xref>
(cf.
<xref rid="bib0415" ref-type="bibr">[83]</xref>
). Although these MEG studies did not manipulate response congruency, they raise the potential importance of changes in communication between brain regions
<xref rid="bib0405" ref-type="bibr">[81]</xref>
. The importance of such interactions was reinforced by a study showing that transcranial magnetic stimulation of the prefrontal cortex abolished repetition suppression in ventrotemporal regions
<xref rid="bib0420" ref-type="bibr">[84]</xref>
.</p>
<p>Although amnesic patients with damage to the medial temporal lobes (MTLs) have long been claimed to show intact priming
<xref rid="bib0425" ref-type="bibr">[85]</xref>
, Schnyer
<italic>et al.</italic>
<xref rid="bib0430" ref-type="bibr">[86]</xref>
found no effect of response congruency in such patients. This is consistent with hippocampal lesions in animals, which typically disrupt learning of arbitrary visuomotor associations
<xref rid="bib0435" ref-type="bibr">[87]</xref>
. One tentative possibility is that S–R bindings are stored in the MTLs (even if not necessarily in a conscious manner) that, when retrieved, interact in the prefrontal cortex with responses generated by component processes in the ventrotemporal cortex. Finally, there are also relevant data from single-cell recording in animals, and neurally plausible computational models are clearly vital to integrate all these types of data
<xref rid="bib0440 bib0445" ref-type="bibr">[88,89]</xref>
.</p>
</boxed-text>
<boxed-text id="tb0020">
<label>Box 4</label>
<caption>
<title>Outstanding questions</title>
</caption>
<p>
<list list-type="simple">
<list-item id="lsti0030">
<label></label>
<p>How do S–R bindings and component processes interact; for example, to affect decision processes that select the final behavioral response?</p>
</list-item>
<list-item id="lsti0035">
<label></label>
<p>How are S–R bindings structured? For example, does a single binding contain multiple stimulus and response representations (as in
<xref rid="fig0010" ref-type="fig">Figure 2</xref>
in main text) or does each stimulus and response representation form a separate ‘binary’ S–R binding? Under what conditions do complex versus specific S–R bindings form? Are simple S–R bindings formed from one learning episode, whereas more complex S–R bindings require more, and more varied, learning episodes?</p>
</list-item>
<list-item id="lsti0040">
<label></label>
<p>How are S–R bindings retrieved? If they contain multiple stimulus and response representations (as in
<xref rid="fig0010" ref-type="fig">Figure 2</xref>
in main text), how do matching and mismatching stimulus representations affect the probability of retrieving a binding? If there are multiple, binary S–R bindings, how do they compete for retrieval – is a single winning binding retrieved or do multiple bindings feed into a decision process?</p>
</list-item>
<list-item id="lsti0045">
<label></label>
<p>What are the limits of stimulus and response representations in S–R bindings? For example, are individual stimulus features bound to responses? How are contexts like task set represented: as part of the same binding or as some kind of index that selects (activates) those S–R bindings that are currently relevant?</p>
</list-item>
<list-item id="lsti0050">
<label></label>
<p>Do different types of S–R binding have different lifetimes (potentially accounting for differences across repetition, negative, and masked priming paradigms) and how long do they last relative to facilitation of component processes?</p>
</list-item>
<list-item id="lsti0055">
<label></label>
<p>How exactly do attention and awareness modulate the encoding and retrieval of S–R bindings?</p>
</list-item>
<list-item id="lsti0060">
<label></label>
<p>How many previous claims for component processes (e.g., in fMRI) reflect S–R bindings instead?</p>
</list-item>
<list-item id="lsti0065">
<label></label>
<p>Which brain regions enable S–R bindings and by what neural mechanisms do they interact with component processes?</p>
</list-item>
</list>
</p>
</boxed-text>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
<li>France</li>
<li>Royaume-Uni</li>
<li>Suisse</li>
</country>
<region>
<li>Angleterre</li>
<li>Canton de Berne</li>
<li>Grand Londres</li>
<li>Île-de-France</li>
</region>
<settlement>
<li>Berne</li>
<li>Londres</li>
<li>Paris</li>
</settlement>
<orgName>
<li>University College de Londres</li>
<li>Université Paris-Descartes</li>
<li>Université de Berne</li>
</orgName>
</list>
<tree>
<country name="Royaume-Uni">
<noRegion>
<name sortKey="Henson, Richard N" sort="Henson, Richard N" uniqKey="Henson R" first="Richard N." last="Henson">Richard N. Henson</name>
</noRegion>
<name sortKey="Horner, Aidan J" sort="Horner, Aidan J" uniqKey="Horner A" first="Aidan J." last="Horner">Aidan J. Horner</name>
<name sortKey="Horner, Aidan J" sort="Horner, Aidan J" uniqKey="Horner A" first="Aidan J." last="Horner">Aidan J. Horner</name>
</country>
<country name="Suisse">
<region name="Canton de Berne">
<name sortKey="Eckstein, Doris" sort="Eckstein, Doris" uniqKey="Eckstein D" first="Doris" last="Eckstein">Doris Eckstein</name>
</region>
<name sortKey="Eckstein, Doris" sort="Eckstein, Doris" uniqKey="Eckstein D" first="Doris" last="Eckstein">Doris Eckstein</name>
</country>
<country name="France">
<region name="Île-de-France">
<name sortKey="Waszak, Florian" sort="Waszak, Florian" uniqKey="Waszak F" first="Florian" last="Waszak">Florian Waszak</name>
</region>
<name sortKey="Waszak, Florian" sort="Waszak, Florian" uniqKey="Waszak F" first="Florian" last="Waszak">Florian Waszak</name>
</country>
<country name="Allemagne">
<noRegion>
<name sortKey="Frings, Christian" sort="Frings, Christian" uniqKey="Frings C" first="Christian" last="Frings">Christian Frings</name>
</noRegion>
</country>
</tree>
</affiliations>
</record>

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