Subcortical Cognition: The Fruit Below the Rind.

Cognitive neuroscience has highlighted the cerebral cortex while often overlooking subcortical structures. This cortical proclivity is found in basic and translational research on many aspects of cognition, especially higher cognitive domains such as language, reading, music, and math. We suggest that, for both anatomical and evolutionary reasons, multiple subcortical structures play substantial roles across higher and lower cognition. We present a comprehensive review of existing evidence, which indeed reveals extensive subcortical contributions in multiple cognitive domains. We argue that the findings are overall both real and important. Next, we advance a theoretical framework to capture the nature of (sub)cortical contributions to cognition. Finally, we propose how new subcortical cognitive roles can be identified by leveraging anatomical and evolutionary principles, and we describe specific methods that can be used to reveal subcortical cognition. Altogether, this review aims to advance cognitive neuroscience by highlighting subcortical cognition and facilitating its future investigation.

The Neurocognition of Developmental Disorders of Language.

Developmental disorders of language include developmental language disorder, dyslexia, and motor-speech disorders such as articulation disorder and stuttering. These disorders have generally been explained by accounts that focus on their behavioral rather than neural characteristics; their processing rather than learning impairments; and each disorder separately rather than together, despite their commonalities and comorbidities. Here we update and review a unifying neurocognitive account-the Procedural circuit Deficit Hypothesis (PDH). The PDH posits that abnormalities of brain structures underlying procedural memory (learning and memory that rely on the basal ganglia and associated circuitry) can explain numerous brain and behavioral characteristics across learning and processing, in multiple disorders, including both commonalities and differences. We describe procedural memory, examine its role in various aspects of language, and then present the PDH and relevant evidence across language-related disorders. The PDH has substantial explanatory power, and both basic research and translational implications.

Child first language and adult second language are both tied to general-purpose learning systems.

Do the mechanisms underlying language in fact serve general-purpose functions that preexist this uniquely human capacity? To address this contentious and empirically challenging issue, we systematically tested the predictions of a well-studied neurocognitive theory of language motivated by evolutionary principles. Multiple metaanalyses were performed to examine predicted links between language and two general-purpose learning systems, declarative and procedural memory. The results tied lexical abilities to learning only in declarative memory, while grammar was linked to learning in both systems in both child first language and adult second language, in specific ways. In second language learners, grammar was associated with only declarative memory at lower language experience, but with only procedural memory at higher experience. The findings yielded large effect sizes and held consistently across languages, language families, linguistic structures, and tasks, underscoring their reliability and validity. The results, which met the predicted pattern, provide comprehensive evidence that language is tied to general-purpose systems both in children acquiring their native language and adults learning an additional language. Crucially, if language learning relies on these systems, then our extensive knowledge of the systems from animal and human studies may also apply to this domain, leading to predictions that might be unwarranted in the more circumscribed study of language. Thus, by demonstrating a role for these systems in language, the findings simultaneously lay a foundation for potentially important advances in the study of this critical domain.

Sequence learning in the human brain: A functional neuroanatomical meta-analysis of serial reaction time studies.

Sequence learning underlies numerous motor, cognitive, and social skills. Previous models and empirical investigations of sequence learning in humans and non-human animals have implicated cortico-basal ganglia-cerebellar circuitry as well as other structures. To systematically examine the functional neuroanatomy of sequence learning in humans, we conducted a series of neuroanatomical meta-analyses. We focused on the serial reaction time (SRT) task. This task, which is the most widely used paradigm for probing sequence learning in humans, allows for the rigorous control of visual, motor, and other factors. Controlling for these factors (in sequence-random block contrasts), sequence learning yielded consistent activation only in the basal ganglia, across the striatum (anterior/mid caudate nucleus and putamen) and the globus pallidus. In contrast, when visual, motor, and other factors were not controlled for (in a global analysis with all sequence-baseline contrasts, not just sequence-random contrasts), premotor cortical and cerebellar activation were additionally observed. The study provides solid evidence that, at least as tested with the visuo-motor SRT task, sequence learning in humans relies on the basal ganglia, whereas cerebellar and premotor regions appear to contribute to aspects of the task not related to sequence learning itself. The findings have both basic research and translational implications.

Procedural memory in infancy: Evidence from implicit sequence learning in an eye-tracking paradigm.

Procedural memory underpins the learning of skills and habits. It is often tested in children and adults with sequence learning on the serial reaction time (SRT) task, which involves manual motor control. However, due to infants' slowly developing control of motor actions, most procedures that require motor control cannot be examined in infancy. Here, we investigated procedural memory using an SRT task adapted for infants. During the task, images appeared at one of three locations on a screen, with the location order following a five-item recurring sequence. Three blocks of recurring sequences were followed by a random-order fourth block and finally another block of recurring sequences. Eye movement data were collected for infants (n = 35) and adults (n = 31). Reaction time was indexed by calculating the saccade latencies for orienting to each image as it appeared. The entire protocol took less than 3 min. Sequence learning in the SRT task can be operationalized as an increase in latencies in the random block as compared with the preceding and following sequence blocks. This pattern was observed in both the infants and adults. This study is the first to report learning in an SRT task in infants as young as 9  months. This SRT protocol is a promising procedure for measuring procedural memory in infants.

Language learning in the adult brain: A neuroanatomical meta-analysis of lexical and grammatical learning.

Language learning as an adult, though often difficult, is quite common. Nevertheless, the neural substrates of this process remain unclear, even though identifying them should clarify how language is learned and could lead to improved success at this endeavor. We addressed this gap by conducting multiple neuroanatomical meta-analyses to synthesize the functional neuroimaging literature of language learning. We focused on learning lexical and grammatical knowledge, two building blocks of language. Lexical and grammatical learning yielded overlapping activation in frontal (e.g., BA 44/45) and posterior parietal regions. Only lexical learning showed ventral occipito-temporal (ventral stream) activation, while only grammatical learning showed basal ganglia (anterior caudate/putamen) activation. To further elucidate the neurocognition of grammar learning, we also tested specific predictions of the declarative/procedural model of language. Consistent with the model, grammar learning predicted to rely especially on declarative memory (e.g., with explicit training) showed hippocampal involvement, while grammar learning predicted to rely particularly on procedural memory (e.g., with implicit training) showed anterior caudate/putamen involvement. Finally, given the prevalence of research on artificial grammars, we performed separate analyses of artificial grammar and non-artificial grammar (e.g., miniature language) paradigms. These yielded overlapping activation, especially in BA 44, underscoring the validity of artificial grammars as models for grammar learning in natural languages. In sum, the study elucidates the empirical and theoretical landscape of language learning and has applied implications.

A dissociation between syntactic and lexical processing in Parkinson's disease.

Parkinson's disease (PD), which involves the degeneration of dopaminergic neurons in the basal ganglia, has long been associated with motor deficits. Increasing evidence suggests that language can also be impaired, including aspects of syntactic and lexical processing. However, the exact pattern of these impairments remains somewhat unclear, for several reasons. Few studies have examined and compared syntactic and lexical processing within subjects, so their relative deficits remain to be elucidated. Studies have focused on earlier stages of PD, so syntactic and lexical processing in later stages are less well understood. Research has largely probed English and a handful of other European languages, and it is unclear whether findings generalize more broadly. Finally, few studies have examined links between syntactic/lexical impairments and their neurocognitive substrates, such as measures of basal ganglia degeneration or dopaminergic processes. We addressed these gaps by investigating multiple aspects of Farsi syntactic and lexical processing in 40 Farsi native-speaking moderate-to-severe non-demented PD patients, and 40 healthy controls. Analyses revealed equivalent impairments of syntactic comprehension and syntactic judgment, across different syntactic structures. Lexical processing was impaired only for motor function-related objects (e.g., naming 'hammer', but not 'mountain'), in line with findings of PD deficits at naming action verbs as compared to objects, without the verb/noun confound. In direct comparisons between lexical and syntactic tasks, patients were better at naming words like 'mountain' (but not words like 'hammer') than at syntactic comprehension and syntactic judgment. Performance at syntactic comprehension correlated with the last levodopa equivalent dose. No other correlations were found between syntactic/lexical processing measures and either levodopa equivalent dose or hypokinesia, which reflects degeneration of basal ganglia motor-related circuits. All critical significant main effects, interactions, and correlations yielded large effect sizes. The findings elucidate the nature of syntactic and lexical processing impairments in PD.

Procedural learning in Tourette syndrome, ADHD, and comorbid Tourette-ADHD: Evidence from a probabilistic sequence learning task.

Procedural memory, which is rooted in the basal ganglia, plays an important role in the implicit learning of motor and cognitive skills. Few studies have examined procedural learning in either Tourette syndrome (TS) or Attention Deficit Hyperactivity Disorder (ADHD), despite basal ganglia abnormalities in both of these neurodevelopmental disorders. We aimed to assess procedural learning in children with TS (n=13), ADHD (n=22), and comorbid TS-ADHD (n=20), as well as in typically developing children (n=21). Procedural learning was measured with a well-studied implicit probabilistic sequence learning task, the alternating serial reaction time task. All four groups showed evidence of sequence learning, and moreover did not differ from each other in sequence learning. This result, from the first study to examine procedural memory across TS, ADHD and comorbid TS-ADHD, is consistent with previous findings of intact procedural learning of sequences in both TS and ADHD. In contrast, some studies have found impaired procedural learning of non-sequential probabilistic categories in TS. This suggests that sequence learning may be spared in TS and ADHD, while at least some other forms of learning in procedural memory are impaired, at least in TS. Our findings indicate that disorders associated with basal ganglia abnormalities do not necessarily show procedural learning deficits, and provide a possible path for more effective diagnostic tools, and educational and training programs.

Hijacking limitations of working memory load to test for composition in language.

Although language depends on storage and composition, just what is stored or (de)composed remains unclear. We leveraged working memory load limitations to test for composition, hypothesizing that decomposed forms should particularly tax working memory. We focused on a well-studied paradigm, English inflectional morphology. We predicted that (compositional) regulars should be harder to maintain in working memory than (non-compositional) irregulars, using a 3-back production task. Frequency, phonology, orthography, and other potentially confounding factors were controlled for. Compared to irregulars, regulars and their accompanying -s/-ing-affixed filler items yielded more errors. Underscoring the decomposition of only regulars, regulars yielded more bare-stem (e.g., walk) and stem affixation errors (walks/walking) than irregulars, whereas irregulars yielded more past-tense-form affixation errors (broughts/tolded). In line with previous evidence that regulars can be stored under certain conditions, the regular-irregular difference held specifically for phonologically consistent (not inconsistent) regulars, in particular for both low and high frequency consistent regulars in males, but only for low frequency consistent regulars in females. Sensitivity analyses suggested the findings were robust. The study further elucidates the computation of inflected forms, and introduces a simple diagnostic for linguistic composition.

Embodied cognition comes of age: A processing advantage for action words is modulated by aging and the task.

Processing action words (e.g., fork, throw) engages neurocognitive motor representations, consistent with embodied cognition principles. Despite age-related neurocognitive changes that could affect action words, and a rapidly aging population, the impact of healthy aging on action-word processing is poorly understood. Previous research suggests that in lexical tasks demanding semantic access, such as picture naming, higher motor-relatedness can enhance performance (e.g., fork vs. pier)-particularly in older adults, perhaps due to the age-related relative sparing of motor-semantic circuitry, which can support action words. However, motor-relatedness was recently found to affect performance in younger but not older adults in lexical decision. We hypothesized this was due to decreased semantic access in this task, especially in older adults. Here we tested effects of motor-relatedness on 2,174 words in younger and older adults not only in lexical decision but also in reading aloud, in which semantic access is minimal. Mixed-effects regression, controlling for phonological, lexical, and semantic variables, yielded results consistent with our predictions. In lexical decision, younger adults were faster and more accurate at words with higher-motor relatedness, whereas older adults showed no motor-relatedness effects. In reading aloud, neither age group showed such effects. Multiple sensitivity analyses demonstrated that the patterns were robust. Altogether, whereas previous research indicates that in lexical tasks demanding semantic access, higher motor-relatedness can enhance performance, especially in older adults, evidence now suggests that such effects are attenuated with decreased semantic access, which in turn depends on the task as well as aging itself. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

The neuroanatomy of developmental language disorder: a systematic review and meta-analysis.

Developmental language disorder (DLD) is a common neurodevelopmental disorder with adverse impacts that continue into adulthood. However, its neural bases remain unclear. Here we address this gap by systematically identifying and quantitatively synthesizing neuroanatomical studies of DLD using co-localization likelihood estimation, a recently developed neuroanatomical meta-analytic technique. Analyses of structural brain data (22 peer-reviewed papers, 577 participants) revealed highly consistent anomalies only in the basal ganglia (100% of participant groups in which this structure was examined, weighted by group sample sizes; 99.8% permutation-based likelihood the anomaly clustering was not due to chance). These anomalies were localized specifically to the anterior neostriatum (again 100% weighted proportion and 99.8% likelihood). As expected given the task dependence of activation, functional neuroimaging data (11 peer-reviewed papers, 414 participants) yielded less consistency, though anomalies again occurred primarily in the basal ganglia (79.0% and 95.1%). Multiple sensitivity analyses indicated that the patterns were robust. The meta-analyses elucidate the neuroanatomical signature of DLD, and implicate the basal ganglia in particular. The findings support the procedural circuit deficit hypothesis of DLD, have basic research and translational implications for the disorder, and advance our understanding of the neuroanatomy of language.

Declarative memory supports children's math skills: A longitudinal study.

Substantial progress has been made in understanding the neurocognitive underpinnings of learning math. Building on this work, it has been hypothesized that declarative and procedural memory, two domain-general learning and memory systems, play important roles in acquiring math skills. In a longitudinal study, we tested whether in fact declarative and procedural memory predict children's math skills during elementary school years. A sample of 109 children was tested across grades 2, 3 and 4. Linear mixed-effects regression and structural equation modeling revealed the following. First, learning in declarative but not procedural memory was associated with math skills within each grade. Second, declarative but not procedural memory in each grade was related to math skills in all later grades (e.g., declarative memory in grade 2 was related to math skills in grade 4). Sensitivity analyses showed that the pattern of results was robust, except for the longitudinal prediction of later math skills when accounting for stable inter-individual differences via the inclusion of random intercepts. Our findings highlight the foundational role of early domain-general learning and memory in children's acquisition of math.

Explicit and implicit second language training differentially affect the achievement of native-like brain activation patterns.

It is widely believed that adults cannot learn a foreign language in the same way that children learn a first language. However, recent evidence suggests that adult learners of a foreign language can come to rely on native-like language brain mechanisms. Here, we show that the type of language training crucially impacts this outcome. We used an artificial language paradigm to examine longitudinally whether explicit training (that approximates traditional grammar-focused classroom settings) and implicit training (that approximates immersion settings) differentially affect neural (electrophysiological) and behavioral (performance) measures of syntactic processing. Results showed that performance of explicitly and implicitly trained groups did not differ at either low or high proficiency. In contrast, electrophysiological (ERP) measures revealed striking differences between the groups' neural activity at both proficiency levels in response to syntactic violations. Implicit training yielded an N400 at low proficiency, whereas at high proficiency, it elicited a pattern typical of native speakers: an anterior negativity followed by a P600 accompanied by a late anterior negativity. Explicit training, by contrast, yielded no significant effects at low proficiency and only an anterior positivity followed by a P600 at high proficiency. Although the P600 is reminiscent of native-like processing, this response pattern as a whole is not. Thus, only implicit training led to an electrophysiological signature typical of native speakers. Overall, the results suggest that adult foreign language learners can come to rely on native-like language brain mechanisms, but that the conditions under which the language is learned may be crucial in attaining this goal.

The influence of language proficiency on lexical semantic processing in native and late learners of English.

We investigated the influence of English proficiency on ERPs elicited by lexical semantic violations in English sentences, in both native English speakers and native Spanish speakers who learned English in adulthood. All participants were administered a standardized test of English proficiency, and data were analyzed using linear mixed effects (LME) modeling. Relative to native learners, late learners showed reduced amplitude and delayed onset of the N400 component associated with reading semantic violations. As well, after the N400 late learners showed reduced anterior negative scalp potentials and increased posterior potentials. In both native and late learners, N400 amplitudes to semantically appropriate words were larger for people with lower English proficiency. N400 amplitudes to semantic violations, however, were not influenced by proficiency. Although both N400 onset latency and the late ERP effects differed between L1 and L2 learners, neither correlated with proficiency. Different approaches to dealing with the high degree of correlation between proficiency and native/late learner group status are discussed in the context of LME modeling. The results thus indicate that proficiency can modulate ERP effects in both L1 and L2 learners, and for some measures (in this case, N400 amplitude), L1-L2 differences may be entirely accounted for by proficiency. On the other hand, not all effects of L2 learning can be attributed to proficiency. Rather, the differences in N400 onset and the post-N400 violation effects appear to reflect fundamental differences in L1-L2 processing.

Knowledge of Statistics or Statistical Learning? Readers Prioritize the Statistics of their Native Language Over the Learning of Local Regularities.

A large body of evidence suggests that people spontaneously and implicitly learn about regularities present in the visual input. Although theorized as critical for reading, this ability has been demonstrated mostly with pseudo-fonts or highly atypical artificial words. We tested whether local statistical regularities are extracted from materials that more closely resemble one's native language. In two experiments, Italian speakers saw a set of letter strings modelled on the Italian lexicon and guessed which of these strings were words in a fictitious language and which were foils. Unknown to participants, words could be distinguished from foils based on their average bigram frequency. Surprisingly, in both experiments, we found no evidence that participants relied on this regularity. Instead, lexical decisions were guided by minimal bigram frequency, a cue rooted in participants' native language. We discuss the implications of these findings for accounts of statistical learning and visual word processing.

Evidence that ageing yields improvements as well as declines across attention and executive functions.

Many but not all cognitive abilities decline during ageing. Some even improve due to lifelong experience. The critical capacities of attention and executive functions have been widely posited to decline. However, these capacities are composed of multiple components, so multifaceted ageing outcomes might be expected. Indeed, prior findings suggest that whereas certain attention/executive functions clearly decline, others do not, with hints that some might even improve. We tested ageing effects on the alerting, orienting and executive (inhibitory) networks posited by Posner and Petersen's influential theory of attention, in a cross-sectional study of a large sample (N = 702) of participants aged 58-98. Linear and nonlinear analyses revealed that whereas the efficiency of the alerting network decreased with age, orienting and executive inhibitory efficiency increased, at least until the mid-to-late 70s. Sensitivity analyses indicated that the patterns were robust. The results suggest variability in age-related changes across attention/executive functions, with some declining while others improve.

Deficits of Learning in Procedural Memory and Consolidation in Declarative Memory in Adults With Developmental Language Disorder.

Purpose This study examined procedural and declarative learning and consolidation abilities in adults with developmental language disorder (DLD) relative to their typical language (TD) peers. Method A total of 100 young adults (age 18-24 years) with (n = 21) and without (n = 79) DLD participated across two sites. Performance measures on a recognition memory task and a serial reaction time task were used to assess declarative and procedural memory, respectively. Performance was measured shortly after learning (8 a.m.) and again after a 12-hr, overnight delay (8 a.m.). Results Linear mixed-effects modeling was used to examine the effects of time and group membership on task performance. For the serial reaction time task, there were significant effects of group (TD > DLD) and time (Day 1 > Day 2), but no interaction between them. For the recognition memory task, there was a significant interaction between group and time, driven by overnight gains in the TD group, combined with stable performance across days by those with DLD. Conclusions In procedural memory, adults with DLD demonstrate a learning deficit relative to adults without DLD, but appear to have comparable retention of learned information. In declarative memory, adults with DLD demonstrate a deficit in the overnight enhancement of memory retrieval, despite typical-like learning exhibited when tested shortly after encoding. Supplemental Material https://doi.org/10.23641/asha.13626485.

Declarative Memory Predicts Phonological Processing Abilities in Adulthood.

Individual differences in phonological processing abilities have often been attributed to perceptual factors, rather than to factors relating to learning and memory. Here, we consider the contribution of individual differences in declarative and procedural memory to phonological processing performance in adulthood. We examined the phonological processing, declarative memory, and procedural memory abilities of 79 native English-speaking young adults with typical language and reading abilities. Declarative memory was assessed with a recognition memory task of real and made-up objects. Procedural memory was assessed with a serial reaction time task. For both tasks, learning was assessed shortly after encoding, and again after a 12-h, overnight delay. We regressed phonological processing ability with memory performance on both days. We found that declarative memory, but not procedural memory, was highly predictive of phonological processing abilities. Specifically, declarative memory scores obtained shortly after learning were associated with non-word repetition performance, whereas declarative memory scores obtained after the overnight delay were associated with phonological awareness. Procedural memory was not associated with either of the phonological processing measures. We discuss these findings in the context of adult participants with mature phonological systems. We examine possible implications for the relationship between declarative memory and phonological processing in adulthood.

Aging affects steaks more than knives: Evidence that the processing of words related to motor skills is relatively spared in aging.

Lexical-processing declines are a hallmark of aging. However, the extent of these declines may vary as a function of different factors. Motivated by findings from neurodegenerative diseases and healthy aging, we tested whether 'motor-relatedness' (the degree to which words are associated with particular human body movements) might moderate such declines. We investigated this question by examining data from three experiments. The experiments were carried out in different languages (Dutch, German, English) using different tasks (lexical decision, picture naming), and probed verbs and nouns, in all cases controlling for potentially confounding variables (e.g., frequency, age-of-acquisition, imageability). Whereas 'non-motor words' (e.g., steak) showed age-related performance decreases in all three experiments, 'motor words' (e.g., knife) yielded either smaller decreases (in one experiment) or no decreases (in two experiments). The findings suggest that motor-relatedness can attenuate or even prevent age-related lexical declines, perhaps due to the relative sparing of neural circuitry underlying such words.