# Evidence for a role of memory in novel word-learning after perinatal stroke

Clément François, Laura Ferreri, Pablo Ripollés, Alfredo Garcia-Alix, Antoni Rodriguez-Fornells, Laura Bosch

► To cite this version:

Clément François, Laura Ferreri, Pablo Ripollés, Alfredo Garcia-Alix, Antoni Rodriguez-Fornells, et al. Evidence for a role of memory in novel word-learning after perinatal stroke. Brain and Language, 2026, 274, pp.105707. 10.1016/j.bandl.2026.105707. hal-04816100

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Evidence for a role of memory in novel word-learning after perinatal stroke

Clément François¹, Laura Ferreri², Pablo Ripollés³,⁴,⁵, Alfredo Garcia-Alix⁶,⁷,⁸, Antoni Rodriguez-Fornells⁹,¹⁰,¹¹,¹²* & Laura Bosch⁶,¹⁰,¹³*

¹ Aix Marseille Univ, CNRS, LPL, Aix-en-Provence, France

² Department of Brain and Behavioral Sciences, University of Pavia, 27100, Pavia, Italy

³ Department of Psychology, New York University, 10003, New York, USA.

⁴ Center for Language, Music, and Emotion (CLAME), New York University, 10003, New York, USA

⁵ Music and Audio Research Laboratory (MARL), New York University, 10003, New York, USA

⁶ Institut de Recerca Sant Joan de Déu (IRSJD), Esplugues de Llobregat, Spain.

⁷ Neonatal Neurology, NeNe Foundation, Madrid, Spain.

⁸ Sociedad Iberoamericana de Neonatología (SIBEN), New Jersey, New Jersey, USA

⁹ Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute-] IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.

¹⁰ Department of Cognition, Development and Educational Science, University of Barcelona, Barcelona, Spain.

¹¹ Catalan Institution for Research and Advanced Studies, ICREA, Barcelona, Spain.

¹² Aix Marseille Univ, IMERA, Marseille, France.

¹³ Institute of Neurosciences (UBNeuro), University of Barcelona, Barcelona, Spain.

Antoni Rodriguez-Fornells, Department of Cognition, Development and Educational Science, University of Barcelona, Campus de Bellvitge - Pavelló de Govern, 08908 L'Hospitalet de Llobregat (Barcelona - Spain). Email: [antoni.rodriguez@icrea.cat](mailto:antoni.rodriguez@icrea.cat)

Laura Bosch, Department of Cognition, Development and Educational Science, University of Barcelona; Institut de Recerca Sant Joan de Déu (IRSJD) and Institute of Neurosciences (UBNeuro), University of Barcelona, Barcelona, Spain. Email: [laurabosch@ub.edu](mailto:laurabosch@ub.edu)

<footnote>*Corresponding authors:</footnote>
**Abstract**

Children with left perinatal arterial ischemic stroke (PAIS) often exhibit language deficits. However, evaluations of learning abilities are scarce. We compared word-referent associative learning and recall performance using a fast-mapping paradigm in a group of 3.5-year-old children with PAIS and in age-matched controls. The task involved a referent selection phase followed by immediate and delayed recall trials of the novel word-object associations. While no between-group differences were observed in the referent selection and immediate recall, children with PAIS showed lower performance in delayed recall of the newly learned associations. These results suggest that word learning difficulties after PAIS may arise due to a memory retention failure rather than to the process of referent selection through disambiguation involved in the fast mapping task. We discuss these findings in relation to the neural bases of infant language acquisition and their implications for clinical practice, particularly in terms of improving lexical acquisition and retention in children with PAIS.

**Keywords:** Perinatal arterial ischemic stroke, word learning, fast-mapping, memory retention
**Introduction**

Perinatal arterial ischemic stroke (PAIS) has an incidence of one in 2300 to 4000 births and affect 5 million people worldwide (Chabrier et al., 2011; Dunbar & Kirton, 2019; Nelson & Lynch, 2004; Lynch, 2009). PAIS can have a long-term negative impact on cognitive development, especially language, often leading to lower academic achievement scores in children who experienced a stroke during the perinatal period, compared to typically developing peers (Ballantyne et al., 2008; Reilly et al., 2013; Westmacott et al., 2010). Furthermore, PAIS is the primary cause of congenital hemiplegia and epilepsy, with around 60% of children with PAIS developing cerebral palsy, 30-60% experiencing epilepsy, 25% showing language delay, and up to 22% exhibiting behavioral disorders (Lee et al., 2005). Interestingly, PAIS over the left hemisphere generally does not lead to post-stroke aphasia (Bates et al., 2001; Stiles et al., 2005), even though subtle language production deficits may be observed (Reilly et al., 2013; Demir et al., 2010), suggesting the possible existence of a developmental form of conduction aphasia characterized by a persistent deficit in speech repetition following neonatal stroke (Northam et al., 2018).

The left middle cerebral artery (MCA) is the blood vessel most affected in PAIS, increasing the risk of suboptimal development of adjacent language-related brain regions (Dunbar & Kirton, 2019). Neuroimaging data collected from newborns with PAIS show that parietal posterior brain regions are the most affected by neonatal stroke (Stephan-Otto et al., 2017; Núñez et al., 2020). Crucially, these lesions can hinder the proper development of the dorsal stream of language processing, which connects the left frontal, parietal, and temporal areas via the arcuate fasciculus (AF; Hickok & Poeppel, 2007; Catani et al., 2007). This pathway is known to support sensory-to-motor transformations (Saur et al., 2008; Schmahmann et al., 2007), verbal short-term memory (Liberman & Mattingly, 1985), syntactic processing (Brauer et al., 2011; Friederici et al., 2006; Berwick et al., 2013) novel word learning (Lopez-Barroso et al., 2013; Rodríguez-Fornells et al., 2009; Assaneo et al., 2019), and working memory processes (Meyer et al., 2014). Interestingly, recent multimodal neuroimaging and behavioral data obtained in 4-year-old children with left PAIS have revealed significant associations between productive aspects of language and both the structural and functional reorganization of the dorsal pathway (i.e., right lateralization of the volume of the AF and right lateralization of the functional connectivity at rest between the superior temporal gyrus and the inferior frontal gyrus; François et al., 2019; 2021). Therefore, PAIS is a good model for studying the brain architecture of language acquisition and processing after early brain lesions. However, to our knowledge, only one single-case study has examined Fast-Mapping (FM) abilities in a preschool-age 3.5-year-old child with left PAIS affecting the supramarginal gyrus, and the superior parietal, and insular cortex extending to the precentral and postcentral gyri (François et al., 2016). In this study, the child was longitudinally followed from 25 to 42 months. Results showed that while cognitive, motor, and language levels
from the Bayley Scales of Infant and Toddler Development (BSID-III) fell within the average
range at 25 months, language scores at 42 months fell below the range. Crucially, in addition to
showing speech production deficits, at that age, the child was impaired in learning novel word-
referent associations via FM.

Successful vocabulary acquisition requires two primary abilities: extracting words from
continuous speech and mapping the novel auditory word forms to their referents (Clerkin & Smith,
2022; François et al., 2017). After a slow initial process in word comprehension beginning around
6 to 9 months of age (Bergelson & Swingley, 2012), and in word production by 12 months of age,
typically developing infants generally exhibit a rapid non-linear growth of their lexical knowledge,
learning an estimated ten new words every two weeks (Axelsson et al., 2021). This increase is
reflected in a dramatical growth of children's expressive vocabulary during their second postnatal
year. It has been estimated that to reach a medium-size vocabulary by pre-school age children
must have learned up to nine new words a day (Samuelson & McMurray, 2017). Indeed, acquiring
meaning through vocabulary learning is a core language-learning mechanism (Bloom, 2000).
Previous research has proposed several learning mechanisms to explain how the word-to-world
mapping problem can be solved (Kuhl, 2004; Davis & Gaskell, 2009; Rodriguez-Fornells et al.,
2009). One of those crucial learning mechanisms involves the ability to map a novel referent to a
novel object with minimal exposure, usually referred to as fast-mapping (FM; Carey & Barlett,
1978; Samuelson & McMurray, 2017; Swingley, 2010; Bloom & Markson, 1998).

In classical FM tasks, children's ability to associate a novel word form with an unfamiliar
object is evaluated through an exposure phase, usually in the presence of already-known objects
in the environment. During this initial learning phase, children need to select or match the correct
referent for the novel word label among objects they already know. Although the underlying
cognitive mechanism supporting referent selection is still under debate, research suggests that it
might rely on disjunctive inference based on mutual exclusivity (Markman & Wachtel, 1988) or
elimination process (Halberda, 2006). Following this exposure phase, children's ability to retain
the association is tested immediately or after a 5-minute delay using a recognition memory test.
Following the first experimental demonstration of FM (Carey & Bartlett, 1978), subsequent
studies suggested that typically developing 2-year-old preschoolers can recall at least one novel
word-object association in an immediate recall test (Spiegel & Halberda 2011). However, learning
more than one word at a time is more challenging, although facilitative manipulations such as
supportive repetition or ostensive naming can induce successful learning and retention in 2- and
3-year-old toddlers (Axelsson & Horst, 2014; Axelsson et al., 2012). For instance, Horst and
Samuelson (2008) found no evidence of successful retention after FM despite "extended mapping"
using explicit repetition and naming (see Cooper et al., 2019 and Vlach, 2019 for a discussion).
Overall, at least two different processes contribute to successful FM: from correct referent
selection to further retention of information (immediate and delayed). Indeed, for some authors,
FM may involve only correct referent selection or matching but not subsequent learning or retention (Vlach, 2019; Spiegel & Halberda, 2011; Cooper et al., 2019).

Regarding the neural bases of FM and considering the associative nature of this learning
process, neuroanatomical models of language learning in adults based on the complementary
learning systems framework have suggested that the early acquisition of new words should be a
process taking place at different time scales from the rapid learning of word-object associations
via medial-temporal lobe encoding (hippocampal-dependent process) to the slow transfer and
build-up of neo-cortical representations that support long-term retention of words via
consolidation (Davis & Gaskell, 2009; McClelland et al., 1995; Coutanche & Thompson-Schill,
2014). By contrast, Sharon and colleagues (2011) provided evidence of preserved learning via
FM in four individuals with amnesia, suggesting that the FM process might reflect a hippocampal-
independent mechanism. This proposal is in line with recent findings showing that rapid cortical
encoding of new information could be independent of the medial temporal lobe (Hebscher et al.,
2019; Brodt et al., 2018), thus indicating that new information could be learned without the need
of engaging classical hippocampal consolidation processes. Nonetheless, recent studies have
challenged the hypothesis that FM is hippocampal-independent (Greve et al., 2014; Smith et al.,
2014; Warren & Duff, 2014), opening questions on the relevance of this mechanism for
vocabulary acquisition (see Cooper et al., 2019 for a critical review). To summarize, there is still
no consensus about the neural bases of FM, probably due to the small number of studies in this
area and the lack of distinction between the two processes involved in learning via FM: referent
selection and delayed retention of information.

In the present study, we aimed to provide new evidence on the neural bases of FM by
evaluating the two processes involved in this type of word learning in a group of children with
PAIS. We compared a group of 3.5-year-old children with PAIS (N = 9; see brain anatomy and
lesions in **Figure 1**) with an age-matched control group (N = 18) tested with a FM paradigm
(modified from Horst & Samuelson, 2008). This specific age was selected for several reasons.
First, children at this age have not acquired reading yet while exhibiting somehow advanced
language production and comprehension skills. Second, the behavioural task we used here was
originally designed for pre-school children (procedure adapted from Horst & Samuelson, 2008,
conducted in 24-month-old infants). Third, FM procedures are well suited to explore word
learning strategies and retention processes after minimal exposure to novel word labels. This skill,
the mechanisms behind it and the factors that can enhance it, have been typically studied in pre-
schoolers (i.e., 2- to 4-year-old children; Jaswal & Markman, 2001; Spiegel & Halberda, 2010;
Bleijlevens et al., 2023), although studies at younger ages (Halberda 2003) and also in adults have
been developed (Cooper et al., 2019; Coutanche & Thompson-Schill, 2014). Fourth, sensitivity
to different types of cues to infer object-names relations may emerge between 3 and 4 years of
age (Nazzi & Gopnik, 2000). The FM paradigm comprised two phases: (i) a word-referent
associative learning phase with supportive repetition of the novel label after correct referent selection, and (ii) recall performance, immediate and delayed, after a five minutes' silent play. Children successively established four novel word-object associations from FM trials in which, after correct referent selection, the experimenter offered supportive learning strategies consisting of three repetitions of the target label embedded in fixed carrier sentences (e.g., Yes, this is a XXX; the XXX is (adjective) and it (verb); It's a XXX, can you say it?), while holding the object closer to the child. The production request of the target label was not repeated when the child remained silent or did not want to produce the novel label. During the referent selection phase, FM trials alternated with trials in which recognition of familiar words was requested to make this referent selection phase less demanding. The two types of trials in this phase involved the presentation of three objects, two familiar and a novel one. This referent selection phase allowed us to evaluate learning by computing the number of correctly selected novel and familiar word-object associations. Crucially, following this referent selection phase, we evaluated both immediate and delayed recall of the new associations to assess the role of memory in FM abilities. During both immediate and delayed recall phases, children were presented again with three objects in each trial, but this time, there were two of the novel objects and a familiar one (either unnamed or not presented in the referent selection phase). Children were requested to select the correct object based on their retention of the previously learned associations. Children's level of performance in this four novel-word learning task was thus not expected to be at ceiling, as processing and retaining multiple label-object mappings in this task is a rather demanding activity (Vlach, 2019; Horst & Samuelson, 2008; Vlach & Sandhofer, 2012).

Considering the brain regions mentioned above, if the processes underlying FM (referent selection and further retention) of the novel words were uniquely hippocampal-dependent, no differences should be observed between patients and controls, as the lesions in the present patient group rarely encompassed medial temporal regions. Specifically, we expected a similar level of performance (number of correct target object selection) in the reference selection phase in the two groups for both novel and familiar word-object associations. However, considering the important role of the left dorsal parieto-temporal frontal network in supporting language learning (Lopez-Barroso et al., 2013; Assaneo et al., 2019; Rodriguez-Fornells et al., 2009; Sierpowska et al., 2016; Vaquero et al., 2016) and working memory processes (Meyer et al., 2014), we expected children with PAIS who were mostly affected in cortical parieto-frontal regions to show impaired recall of newly learned word-object associations. This effect should be reflected by a lower level of performance (i.e., lower number of correctly recalled target objects) for children with PAIS compared to matched controls in the recall phases, especially in the delayed one.
# Material and Methods

## Participants

Nine children with symptomatic PAIS (six of them with lesions over the left hemisphere, 2 with bilateral lesions, 1 with lesions over the right hemisphere; two females) participated in the study. These children were part of a more extensive prospective, observational, multicenter study about acute symptomatic PAIS. At the time of testing, all but two children received speech therapy every week (L2 and L6). Symptomatic PAIS was defined as the finding of an ischemic lesion by magnetic resonance imaging (MRI) in the territory of the middle cerebral artery (MCA, anterior cerebral artery [ACA], and posterior cerebral artery [PCA]) in an infant presenting with seizures, recurrent apnea or acute neurological deficit during the first days of life. Infants with (i) clear signs of tissue loss or atrophy in MRI suggestive of an old infarction that occurred before birth; (ii) vascular malformation; (iii) congenital or chromosomic anomalies; (iv) metabolic or infectious diseases; (v) complex heart congenital diseases; or (vi) infants with extra corporeal membrane oxygenation (ECMO), were excluded from the study. MRI-based diagnostics were performed on anatomical data acquired on a 1.5 T whole-body MRI scanner with a specific neonatal head coil within seven days after the neurologic symptoms. These MRI data allowed for the classification of the lesions according to the arterial territory involved (i.e., four segments: M1-M4). The classification of each infarct was obtained by two independent neurologists blind to the clinical data. Discrepancies in the classification of the PAIS were discussed and solved by consensus at joint revaluation among three observers: AGA and two neurologists blind to the clinical data. Motor impairment was considered when infants had clear clinical signs of monoplegia/ hemiplegia (Gross Motor Function Classification System, GMFCS at least I and/or Bimanual Fine Motor Function, BFMF at I level). Infants with minor abnormalities such as precocious handedness and mild abnormalities of tone or reflexes that did not interfere with functions were not considered to have a motor impairment. MRI data was also acquired at 3.5 years (SD = 0.26) using a 1.5 T whole body scanner (GE Signa HD) to assess the state of the residual lesion and to obtain functional and structural data reported elsewhere (François et al., 2016, 2019). T1-weighted high-resolution anatomical images (magnetization-prepared rapid acquisition gradient echo sequence; TR 12.39 ms, TE 5.22 ms, slice thickness 0.4297 mm, 1-mm in-plane resolution, 180 slices, matrix size 512*512) demonstrated that all children had infarctions of the MCA affecting several brain regions (Table 1; Figure 1).
<table><thead><tr><th>Patient code</th><th>Age at test (months)</th><th>Gender</th><th>Gestational age at birth (weeks)</th><th>Birth weight (g)</th><th>Clinical debut (hours of age)</th><th>Age of MRI diagnostic (days)</th><th>Vascular territory</th><th>Stroke Volume at birth (mL)</th><th>Motor impairment (Hemiplegia)</th><th>Epilepsy*</th></tr></thead><tbody><tr><td>L1</td><td>48</td><td>M</td><td>41</td><td>3160</td><td>Clonic Seizures at 12 hours</td><td>4 days</td><td>M2 L</td><td>18890</td><td>No</td><td>No</td></tr><tr><td>L2</td><td>48</td><td>F</td><td>41</td><td>2960</td><td>Clonic Seizures at 26 hours</td><td>10 days</td><td>M4 L</td><td>47428</td><td>Yes</td><td>No</td></tr><tr><td>L3</td><td>50</td><td>M</td><td>40</td><td>3560</td><td>Clonic Seizures at 48 hours</td><td>20 days</td><td>M1 Post-bifurcation L</td><td>17588</td><td>No</td><td>No</td></tr><tr><td>L4</td><td>41</td><td>F</td><td>41</td><td>2600</td><td>Clonic Seizures at 18 hours</td><td>4 days</td><td>M2 sup L</td><td>27882</td><td>No</td><td>No</td></tr><tr><td>L5</td><td>42</td><td>M</td><td>39</td><td>3340</td><td>Clonic Seizures at 24 hours</td><td>5 days</td><td>M1 Post-bifurcation L</td><td>36512</td><td>No</td><td>No</td></tr><tr><td>L6</td><td>49</td><td>M</td><td>40</td><td>3025</td><td>Clonic Seizures at 41 hours</td><td>5 days</td><td>M1 Post-bifurcation L</td><td>23509</td><td>Yes</td><td>No</td></tr><tr><td>L/R1</td><td>41</td><td>M</td><td>39</td><td>3000</td><td>Clonic Seizures at 16 hours</td><td>8 days</td><td>M3 bilateral post</td><td>30637</td><td>No</td><td>No</td></tr><tr><td>L/R2</td><td>41</td><td>M</td><td>39</td><td>3240</td><td>Clonic Seizures at 24 hours</td><td>6 days</td><td>M1 Post-bifurcation R & M4 sup L</td><td>15332</td><td>No</td><td>No</td></tr><tr><td>R1</td><td>41</td><td>M</td><td>41</td><td>3045</td><td>Clonic Seizures at 72 hours</td><td>5 days</td><td>M2 sup R</td><td>7063</td><td>Yes</td><td>No</td></tr></tbody></table>

* Epilepsy = at least two recurrent and unprovoked seizures.

<caption>**Table 1.** Children demographic data and lesions main features.</caption>
<figure><img src="image_2.png" /><figcaption>**Figure 1:** MRI scans obtained at 3.8 years of age in 6 children with Left and three children with Right or Bilateral PAIS. The figure depicts the structural lesions in native space using a T1-weighted image (axial view). The lesions can be seen as hypo-intense areas and are highlighted with a red circle. Neurologic convention is used.</figcaption></figure>

A typically developing age-matched control group of children (N = 18, 7 males) from similar cultural and language backgrounds, educational levels, and geographical areas was also tested. All the control children showed a right-hand preference at the time of the study. Socio-economic status was determined by the highest educational level attained by each parent and was assessed in all participants. Levels ranging from 1 to 4 reflected no school, primary school, secondary school, and university degree, respectively. No significant differences were found regarding age: control group (mean = 44.1 months; SD = 5.04) versus patients (mean = 44.5 months; SD = 4.03; *U* = 81.5; *P* = 1). No significant differences were found regarding the socio-economic status (*t* = .84; *P* = .35). The parents of the children received information on the study in written and spoken form, and their written consent was obtained before the study began. The study was approved by the Ethics Committee of the Hospital Sant Joan de Déu (CEIC PIC-85-13) in accordance with the Declaration of Helsinki.

*Standard neuropsychological testing*

*Cognitive functions* in the domains of memory and learning, visuospatial processing, sensorimotor skills, and language were assessed using the NEPSY-II battery (Korkman et al., 2007, Spanish adaptation), a standardized neuropsychological battery used in clinical research to identify areas or domains that are preserved and domains that are affected. The battery has specific subtests suitable for children from 3 years of age. Scaled scores between 8-12 indicate the values expected in typically-developing children. These are the subtests that were employed to assess specific skills in each of the four areas we selected for evaluation: a) language (subtests: comprehension of instructions; body part naming and identification; word generation; phonological processing; speeded naming); b) memory and learning (subtests: memory for designs; narrative memory; sentence repetition); c) visuospatial (subtests: block construction; design copying); and d) sensorimotor processing (subtests: imitating hand positions, visuomotor
precision). Raw scores for each sub-test were converted into scaled scores and compared to
normative values (mean = 10, SD = 2).

FM task

Word-learning ability was assessed with a task designed to measure fast mapping and recall of multiple novel word-object associations. This task was adapted from Horst and Samuelson (2008, experiment 1). The task involved a “referent selection” or “learning” phase, during which ostensive naming and the experimenter provided labelling of the target elements after correct selection by the participant. This initial referent selection phase was followed by two recall phases, one immediately after the referent selection phase and the other after a 5-minute delay (i.e., immediate and delayed recall phases). During this 5-minute delay and before the second recall phase, the participant performed a silent non-linguistic sensorimotor manipulative task, as done in the original version of the task (Horst & Samuelson, 2008; see Bosch, APAL Lab documents and testing material for details on the procedure).

<figure><img src="image_3.png" /><figcaption>**Figure 2:** Examples of the novel target objects used in the present experiment (top view).</figcaption></figure>

The labels used for the four novel words were all phonotactically correct pseudowords in Spanish, involving different syllabic lengths (one monosyllabic, one disyllabic, and two trisyllabic words) and very distinctive at the segmental level ([gomi], [flas], [binoko], and [kufeta]). Each label was associated with a distinct novel object. These four objects had been selected from a set of pet toys or non-figurative objects, distinctly differing in their shape, color, material, and textures (see **Figure 2**). The twelve familiar words and objects used in this task were the following: a flower, a cow, a horse, a car, a feeding bottle, a ball, a cap, a spoon, a small plate, a hen, a plane, and a children's book. Among the twelve familiar objects, eight were used in the referent selection phase, but only four of them were named and requested. The remaining four familiar objects served as distractors. The four unnamed objects and those not presented in the
referent selection phase were used and requested in the recall phases. All trials involved the presentation of three objects, but the distribution of familiar and novel objects differed depending on the phase with one novel object being presented together with two familiar ones during the FM phase and two novel objects together with two familiar ones during the recall phases.

The task began with a single practice trial, involving two familiar and a novel object so as to familiarize the participant with the game to be played and the task demands. In this practice trial "shoe" and "cat" were used as familiar objects and a non-figurative unfamiliar one to be named "din" were used and not presented again in any of the following task phases (learning and recall). The child was requested to point to the "din". If the answer was correct, verbal feedback was given to clearly show successful referent selection. If an incorrect pointing was produced (i.e., selecting either the cat or the shoe), then the experimenter modified the initial request, this time guiding the child towards the correct referent selection for the novel label "din", that is, she began requesting the child to point to the "cat", then the "shoe" and finally the "din", so as to be able to confirm that this final selection had been successful. In this practice trial, it was important to make sure that the child had understood the disambiguation mechanism that was to be used in the learning phase trials.

Then, the referent-selection phase (i.e., FM or learning phase) began. It included eight trials, and each trial involved the presentation of one novel object and two familiar ones. The first trial of that phase involved a request of one of the familiar objects. In the following seven trials, the experimenter successively alternated requests of novel and familiar objects so that, at the end, four familiar objects (out of eight that were presented) and the four novel ones were requested during the learning phase. In trials requesting to point to a novel object, after correct object selection, the experimenter produced a fixed set of utterances naming the novel object twice and ending with a request for the child to name it after her (e.g., "Yes, this is a *flas*. The *flas* is small and it makes some noise. It's a *flas*, can you name it?"). In case of incorrect referent selection (i.e., pointing to a familiar object), the response was registered but the trial was repeated following the same procedure as in the initial practice trial, favouring the correct referent selection by the child and the novel name repetitions produced by the experimenter. This ostensive naming procedure was used in this referent selection (or learning) phase to maximize word learning retention so that responses in the immediate and delayed recall phases could reliably be above chance level in such a demanding learning context.

The FM or learning phase was followed by an immediate recall test with eight trials, in which the experimenter requested children to point or select twice each of the four novel name-novel objects previously mapped, presented in the same order as in the learning phase. In this way, the same temporal distance for all four novel words was maintained, but the context in which the objects were presented was modified. First of all, the triplets now involved two novel objects
and just a familiar one, so word-referent task demands were more challenging and correct answers could not be given if the child had not retained the previous word-referent mappings. In the first four trials, familiar objects had been seen before but not requested in the previous learning phase (they were unnamed familiar objects). In the second set of four trials, familiar objects had not been seen before. The format of the request was slightly modified: Children were requested to point to a novel object and then to the familiar one in that trial, so that positive feedback could be offered relative to the correct selection of that familiar object. Crucially along this phase, the four novel objects were requested twice but in two different contexts, each involving different foils, thus providing the necessary experimental control to adequately assess children's multiple-word learning capacity and increasing task validity (see Axelsson & Horst, 2013). Finally, after a delay of 5 minutes during which the child was engaged in a silent, non-linguistic sensorimotor manipulative task, the delayed recall phase was administered, repeating the same sequence of trials as in the immediate recall phase (see **Figure 3** for an example of trials involving a novel word/object in different phases of the task). Each correct selection of a newly learned word scored 1 (maximum score 8). The coding of children's answers was done online (the experimenter marked the answer on a recording list not visible to the participant), but also checked offline from a video recording of the session with a small camera that displayed the tray with the three objects and the face/hands of the child. Answers were scored as correct based on the first stable look/point of the participant; an independent coder who was blind to the requested object was used to confirm the correct scoring in this procedure.

<figure><img src="image_4.png" /><figcaption>**Figure 3.** Schematic illustration of the experimental procedure involving an initial fast mapping followed by two test phases (immediate and delayed recall). The images show different displays involving one of the novel objects. In the referent selection phase, trials requesting the novel object and one familiar object were alternated. During the first test phase, children were immediately evaluated on their recall of the four novel name-object pairs. On the first 4 trials the familiar object was one already seen in the referent selection phase but not named; on the last four trials, a familiar object, previously unseen, was used. After completing a 5-minute non-linguistic task, children were re-tested on their delayed recall of the same novel name-objects pairs.</figcaption></figure>

*Statistical analysis*
As recommended for individual-level analyses with small control groups (Crawford & Howell, 1998), we compared the data from each child with PAIS with the average level of performance of the control group. The comparisons were performed using a modified *t*-test, specifically designed to compare an individual to a small sample of control participants (Crawford, Garthwaite, & Porter, 2010). We also performed statistical analyses at the group level using non-parametric Mann-Whitney tests for independent samples on all measures.

# RESULTS

## Neuropsychological testing – NEPSY II

Composite scores corresponding to four specific cognitive domains of the NEPSY-II (i.e., Language, Memory and Learning, Visuospatial, and Sensorimotor Processing; see **Methods**) were computed by averaging the individual scaled scores obtained in the target subtests from each domain. PAIS participants, as a group (N = 9), although relatively low, the mean score in the language domain (mean = 8.58; SD = 1.06) fell within the normal range. Similar values were obtained in the memory and learning (mean = 8.63; SD = 1.12), and sensorimotor domains (mean = 8.39; SD = 1.23; see **Figure 4**). However, the mean composite score in the visuospatial processing domain was below the normal range with a mean value < 8, corresponding to percentile values 11-25. We used the Mann-Whitney test to evaluate possible differences as a function of the lesion side. We compared the performance of children with a left lesion (N = 6) to those with a bilateral/right lesion (N = 3). We found a significant difference for the memory and learning domain, which included scaled scores from the narrative memory, sentence repetition, and memory for designs subtests. Children with a left lesion (Mdn = 3) performed significantly lower than children with a right lesion (Mdn = 6; *U* < .001, *Z* = -2.343, *P* = .024; see **Figure 4**). No significant differences according to the lesion side were found for the other composite scores (all *P*-s > .05).

<figure><img src="image_5.png" /><figcaption>**Figure 4:** NEPSY-II evaluation. Means and SDs barplots of the composite scores from the NEPSY-II (language, memory and learning, visuospatial and sensorimotor processing) in the group of children with PAIS. The gray slots indicate the normative scores range (8–12). L (circles), children with a left-hemispheric lesion. R (triangles), children with a right or bilateral hemispheric lesion.</figcaption></figure>
## Novel word learning - FM

Figure 5 shows the level of performance in the FM and test phase for the two groups of children. Concerning the FM (referent selection) phase, most of the children performed adequately for both conditions (familiar and novel objects), with a few exceptions. Specifically, all children from both groups correctly selected the referents for familiar words in all trials (Figure 5A). For novel words (Figure 5B), both groups correctly selected the four novel objects except patient L3, who selected only 2 out of 4 items and three children from the control group selecting 3 out of 4 objects. This result shows that the demands of the task at the tested age are still relatively high, in spite of the ostensive modality of the procedure and the repetition of the trial when needed, thus favoring immediate recall of the novel word-object associations. No between-group difference was observed.

Concerning the recall phases, we found no difference in the immediate recall phase when comparing the individual patients' scores to the average of the control group. However, in the delayed recall phase, six out of nine children with PAIS performed lower than controls, although not significant (see Table 2). Interestingly, it is worth noting that out of these six children, five of them had a left lesion. These results were confirmed at the group level: while no differences were found in the immediate retention phase (Figure 5C), children with PAIS performed significantly lower than the controls in the delayed recall phase ($U = 41.5; P < .037; Figure 5D$). No differences were observed as a function of lesion side in both the immediate and delayed recall phases (all $Ps > .05$).

<figure><img src="image_6.png" /></figure>

**Figure 5.** Behavioral FM data showing the individual scores for children with PAIS (red) and controls (black) in the referent selection phase for familiar (A) and novel words (B) and in the immediate (C) and delayed (D) recall tests. The bars show the mean, and the SEM. \* indicates a significant difference at $P < .05$. Red circles and triangles depict individual data from patients with left or right/bilateral lesion respectively. Black dots represent results from the control group.
Finally, we compared the level of performance between the two tests (immediate and delayed) separately for each group. Interestingly, while no difference was observed between immediate and delayed recall performance in the group of control children ($t_{17} = 0.308; P = .762$), there was a clear drop in performance for the group of children with PAIS showing lower recognition in the delayed than in the immediate test phase ($t_8 = 3.83; P = .005$). No effect of lesion side was observed ($t_7 = 0.32; P = .38$).

<table><caption>**Table 2.** Behavioural data for immediate and delayed recall phases showing the percentage of correctly recalled items for the control group (N=18) and for each child with PAIS. \* indicates individual scores with a P value of .08 when compared to the control group according to the Crawford modified *t*-test (one-tailed). \*\* indicates individual scores with a P value of .01 when compared to the control group according to the Crawford modified *t*-test (one-tailed).</caption><thead><tr><th></th><th>Immediate recall<br>(% of CR)</th><th>Delayed recall<br>(% of CR)</th></tr></thead><tbody><tr><td>Controls</td><td>70.8 (19.6)</td><td>69.4 (13)</td></tr><tr><td>L1</td><td>75</td><td>50 (*)</td></tr><tr><td>L2</td><td>62.5</td><td>50 (*)</td></tr><tr><td>L3</td><td>62.5</td><td>50 (*)</td></tr><tr><td>L4</td><td>100 (*)</td><td>100 (**)</td></tr><tr><td>L5</td><td>87.5</td><td>50 (*)</td></tr><tr><td>L6</td><td>62.5</td><td>50 (*)</td></tr><tr><td>L/R1/bilateral</td><td>75</td><td>75</td></tr><tr><td>L/R2/bilateral</td><td>100</td><td>62.5</td></tr><tr><td>R1</td><td>75</td><td>50 (*)</td></tr></tbody></table>

## Discussion

Here, we explored the impact of PAIS on learning novel word-referent associations, one of the core processes of language acquisition. We tested a small group of 3.5-year-old children with PAIS using a FM paradigm that allowed us to assess both referent selection and information retention processes. We found that PAIS directly impacted the delayed recall of newly learned associations while leaving referent selection and immediate recall performance spared. The present results suggest an essential role of memory in the word learning deficits observed after PAIS, but with preserved capacities to correctly match and select a referent for a novel word label in the presence of already known objects.
In the FM phase, we found no between-group differences in the ability to map novel words to novel objects (Figure 5B) or recognize familiar word-object associations (Figure 5A). This result supports the idea that the fronto-parietal-temporal lesions observed in the group of patients did not interfere with the process of inference requested for correctly selecting the reference in the exposure phase. Importantly, these results extend our previous PAIS single-case study, in which a child with a clear lesion affecting the left arcuate fasciculus was assessed using the same FM task and showed spared mapping but impaired performance in the immediate and delayed recall tasks (François et al., 2016). The current findings from the referent selection task were remarkably consistent across all participants, even with the small sample size. Nonetheless, at the individual level, one child with PAIS (L3) incorrectly selected the novel items, suggesting a difficulty in forming associations despite ostensive naming. Interestingly, this participant exhibited composite scores in visuospatial processing, learning and memory, and sensorimotor domains that were below the normal range, with mean values < 8, corresponding to the 11<sup>th</sup>-25th percentile. The participant's inability to solve the selection phase is particularly surprising, given the performance of the other patients in the sample. This observation points to the potential effect of the lesion on high-level, domain-general mechanisms affecting learning and reasoning abilities, likely disrupting the generation of appropriate inferences. Indeed, elementary forms of logical representations may contribute to inference and problem-solving (Cesana-Arlotti et al., 2018). Therefore, this impairment may have cascading effects on language development (as evidenced by the low scores in neuropsychological tests of patient L3; see Figure 4).

Interestingly, a different pattern of results emerged when focusing on the performance in the immediate and delayed recall tests. While no differences were found in the immediate recall phase, children with PAIS performed significantly lower than controls in the delayed recall phase when considered as a group. Interestingly, recent evidence show that 3- to 5-year-old healthy children are sensitive to the learning context and may use associative matrices to support word mapping (Knabe & Vlach, 2023). Overall, these observations suggest that PAIS may not impair the learning process *per se*, and further confirm that mapping and recall are distinct processes, although potentially related (Kucker et al., 2015). Indeed, such a dissociation has been demonstrated in previous research where participants who showed preserved referent selection during the mapping were not necessarily good at recall (Horst & Samuelson, 2008). Several authors have attributed these forgetting effects to infants' reduced capacity to encode long-term information due to the immaturity of the hippocampal system, especially during the first two years of life (Utsunomiya et al., 1999; Keresztes et al., 2018). However, our data do not support this view, as most of the lesions in our patients affected cortical temporal-parietal-frontal networks, sparing the hippocampus. Thus, the idea that PAIS participants may exhibit greater forgetting due to the immaturity of medial temporal networks seems unlikely in our sample. Nevertheless, it remains possible that PAIS indirectly impacts the integration and formation of new memories at
the cortical level, potentially disrupting the transfer of information from the hippocampal system
to neocortical regions. In this case, such disruptions could be a consequence of perinatal stroke
and the associated reduction in connectivity between hippocampal and cortical regions.

Overall, the present results support the hypothesis that lesions near the white-matter tract connecting left temporo-parietal and frontal regions (the arcuate fasciculus, see figure 6A in François et al., 2019 for evidence of disrupted left arcuate fasciculus in this group) may disrupt vocabulary acquisition. Extensive research over the last decade has converged on the crucial role of this left hemisphere dorsal language pathway in learning and retaining newly acquired phonological information (Catani et al., 2005; Schmahmann et al., 2007; Hickok & Poeppel, 2007; Rodriguez-Fornells et al., 2009). For instance, previous studies have shown that the integrity of the arcuate fasciculus, a key component of the phonological loop, is involved in word learning during speech segmentation tasks (Lopez-Barroso et al., 2013; Assaneo et al., 2019), in the ability to learn foreign-language sounds (Vaquero et al., 2016; Golestani & Zatorre, 2004), in repeating new words during awake surgery (Sierpowska et al., 2017), and in working memory processes (Meyer et al., 2014). Notably, recent longitudinal evidence from healthy children aged 4 to 10 years has revealed a clear association between the white-matter microstructure of the left posterior and direct segments of the arcuate fasciculus and vocabulary growth rate (Su et al., 2018).

The present data provide new evidence on the importance of preserving the dorsal pathway involving the arcuate fasciculus for the proper long-term retention of information during FM. Lesions of these brain regions in PAIS could represent a significant predictor of potential delays in the development of language milestones, particularly vocabulary acquisition. Indeed, a recent voxel-based lesion-symptom MRI mapping study of a large cohort of PAIS showed an association between the requirement for speech therapy and lesions involving the left supramarginal gyrus, a region closely linked to the arcuate fasciculus (Núñez et al., 2020; see also Northam et al., 2018, for similar results).

Future research should be conducted to design language interventions that could mitigate
the negative effects of PAIS. One critical factor for information retention and recall at these ages
is repetition, which might compensate for the protracted development of the hippocampal
networks and consequent forgetting (Horst, 2013). Interventions designed to improve retention
by preventing forgetting mechanisms could consider reinforcing new episodic traces and creating
richer encoding contexts (combined with repetition) to strengthen the various features associated
with novel labels (see Horst, 2013, for evidence from contextual repetition in learning novel
words from children's storybooks). The enriched episodic memory traces may facilitate later
retrieval and language production. This idea aligns with perspectives proposing that word learning
is a slow, gradual associative process requiring multiple exposures to word-referent pairing to
build proper word-reference representations (a sort of “slow mapping”; Smith & Yu, 2008; McMurray et al., 2012; Rodriguez-Fornells et al., 2009).

Our study presents some limitations. First, the sample size of children with PAIS is small, which is an inherent problem when studying rare neonatal conditions (François et al., 2021). Consequently, even though designs involving small number participants are still frequent in clinical research (Smith & Little, 2018), the present results may lack of generalizability power both due to this small sample size and heterogeneity of lesion location and size. Further studies with larger sample sizes and more precise lesion localization and classification are needed to specify the deficits observed after PAIS according to the type of lesion. Second, we evaluated referent selection and retention but not generalization, another crucial process required for vocabulary acquisition (Kucker & Seidler, 2023). Future studies may implement a generalization task to have a better understanding of core word learning mechanisms in this population. Finally, we evaluated the children only once thus limiting the developmental contribution of our results.

In summary, we report the first evaluation of FM abilities and fine-grained assessments of cognitive and language functions in four-year-old preschool children with congenital lesions. We provide evidence for the critical role of memory in triggering typical vocabulary growth. These results suggest that poor performance in word learning in the face of a congenital lesion may arise due to memory retention failures rather than to the difficulties in disambiguation processes or uncertainty in selecting the target reference during FM.

## Acknowledgments

We warmly thank all the children and their families for their enthusiasm in participating in the present study. We dedicate this article to the memory of our dear friend and colleague Alfredo García-Alix, who sadly passed away while we were completing this work. His invaluable help, enthusiasm, and inspiration were instrumental to this study on perinatal stroke, as well as to the many projects we collaborated on over the past decade. We continue to be deeply inspired by his dedication to the study of perinatal stroke and, more broadly, to the field of neonatal neurology. His legacy will remain a guiding force in our work. This research was co-funded by FEDER funds/European Regional Development Fund (ERDF)-"A Way to Build Europe". This research was also supported by a grant from the Bial Foundation (Bursaries for Scientific Research) awarded to ARF, by the Catalan Government (PERIS2017) to CF, an FPU program AP2010-4179 to PR, Spanish MICINN projects (PSI 2011-25376; PID 2021-128159NB-100) to LB and an ISCIII project to AGA (IP-081366). ARF has been also supported by the FIAS fellowship Program, co-funded by the European Commission, Marie-Skłodowska-Curie Actions - COFUND Program (Grant #945408). Finally, this work, carried out within the Institute of Convergence ILCB (ANR-16-CONV-0002), has benefited from support from the French government (France 2030), managed by the French National Agency for Research (ANR) and the Excellence Initiative of Aix-Marseille University (A*MIDEX).

## Competing Interests

The authors declare that they have no competing interests.

## Data availability statement

Data available on request.
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<table><caption>**Table 1.** Children demographic data and lesions main features.</caption><thead><tr><th>Patient code</th><th>Age at test (months)</th><th>Gender</th><th>Gestational age at birth (weeks)</th><th>Birth weight (g)</th><th>Language at home</th><th>Clinical debut (hours of age)</th><th>Age of MRI diagnostic (days)</th><th>Vascular territory</th><th>Stroke Volume at birth (mL)</th><th>Motor impairment (Hemiplegia)</th><th>Epilepsy*</th></tr></thead><tbody><tr><td>L1</td><td>48</td><td>M</td><td>41</td><td>3160</td><td>Spanish/Catalan</td><td>Clonic Seizures at 12 hours</td><td>4 days</td><td>M2 L</td><td>18890</td><td>No</td><td>No</td></tr><tr><td>L2</td><td>48</td><td>F</td><td>41</td><td>2960</td><td>Spanish/Catalan</td><td>Clonic Seizures at 26 hours</td><td>10 days</td><td>M4 L</td><td>47428</td><td>Yes</td><td>No</td></tr><tr><td>L3</td><td>50</td><td>M</td><td>40</td><td>3560</td><td>Spanish/Catalan</td><td>Clonic Seizures at 48 hours</td><td>20 days</td><td>M1 Post-bifurcation L</td><td>17588</td><td>No</td><td>No</td></tr><tr><td>L4</td><td>41</td><td>F</td><td>41</td><td>2600</td><td>Spanish/Catalan</td><td>Clonic Seizures at 18 hours</td><td>4 days</td><td>M2 sup L</td><td>27882</td><td>No</td><td>No</td></tr><tr><td>L5</td><td>42</td><td>M</td><td>39</td><td>3340</td><td>Spanish/Catalan</td><td>Clonic Seizures at 24 hours</td><td>5 days</td><td>M1 Post-bifurcation L</td><td>36512</td><td>No</td><td>No</td></tr><tr><td>L6</td><td>49</td><td>M</td><td>40</td><td>3025</td><td>Spanish</td><td>Clonic Seizures at 41 hours</td><td>5 days</td><td>M1 Post-bifurcation L</td><td>23509</td><td>Yes</td><td>No</td></tr><tr><td>L/R1</td><td>41</td><td>M</td><td>39</td><td>3000</td><td>Spanish/Catalan</td><td>Clonic Seizures at 16 hours</td><td>8 days</td><td>M3 bilateral post</td><td>30637</td><td>No</td><td>No</td></tr><tr><td>L/R2</td><td>41</td><td>M</td><td>39</td><td>3240</td><td>Spanish/Catalan</td><td>Clonic Seizures at 24 hours</td><td>6 days</td><td>M1 Post-bifurcation R &amp; M4 sup L</td><td>15332</td><td>No</td><td>No</td></tr><tr><td>R1</td><td>41</td><td>M</td><td>41</td><td>3045</td><td>Spanish/Catalan</td><td>Clonic Seizures at 72 hours</td><td>5 days</td><td>M2 sup R</td><td>7063</td><td>Yes</td><td>No</td></tr></tbody></table>

<footnote>* Epilepsy = at least two recurrent and unprovoked seizures.</footnote>