Implicit Associative Learning Research Articles

Reduced Implicit but not Explicit Knowledge of Cross-Situational Statistical Learning in Developmental Dyslexia.

Although statistical learning (SL) has been studied extensively in developmental dyslexia (DD), less attention has been paid to other fundamental challenges in language acquisition, such as cross-situational word learning. Such investigation is important for determining whether and how SL processes are affected in DD at the word level. In this study, typically developed (TD) adults and young adults with DD were exposed to a set of trials that contained multiple spoken words and multiple pictures of individual objects, with no information about word-referent correspondences provided within a trial. Nonetheless, cross-trial statistical relations could be exploited to learn word-referent mappings. The degree of within-trial reference uncertainty and the novelty of to-be-learned objects (novel or familiar) were varied under different learning conditions. The results show that across all conditions, young adults with DD were significantly impaired in their ability to exploit cross-trial regularities in co-occurring visual-auditory streams to discover word-referent mappings. Observed impairments were most pronounced when within-trial reference uncertainty was the highest. Subjective measures of knowledge awareness revealed greater development of implicit but not explicit knowledge in the TD group than in the DD group. Together, these findings suggest that the SL deficit in DD affects fundamental language learning challenges at the word level and points to greater reliance on explicit processes due to impaired implicit associative learning among individuals with DD. Such a deficit is likely to influence spoken language acquisition, and in turn affect literacy skills, in people with DD.

Implicit threat learning involves the dorsolateral prefrontal cortex and the cerebellum

Background/ObjectiveMost studies investigating the neural correlates of threat learning were carried out using an explicit Pavlovian conditioning paradigm where declarative knowledge on contingencies between conditioned (CS) and unconditioned stimuli (US) is acquired. The current study aimed at understanding the neural correlates of threat conditioning when contingency awareness is limited or even absent. MethodWe conducted an fMRI report of threat learning in an implicit associative learning paradigm called multi-CS conditioning, in which a number of faces were associated with aversive screams (US) such that participants could not report contingencies between the faces and the screams. ResultsThe univariate results showed support for the recruitment of threat-related regions including the dorsolateral prefrontal cortex (dlPFC) and the cerebellum during acquisition. Further analyses by the multivariate representational similarity technique identified learning-dependent changes in the bilateral dlPFC. ConclusionOur findings support the involvement of the dlPFC and the cerebellum in threat conditioning that occurs with highly limited or even absent contingency awareness.

Age group differences in learning-related activity reflect task stage, not learning stage

Healthy aging is accompanied by declines in the ability to learn associations between events, even when their relationship cannot be described. Previous functional magnetic resonance imaging (fMRI) studies have attributed these implicit associative learning (IAL) deficits to differential engagement of the hippocampus and basal ganglia in older relative to younger adults in early and late stages of the task, respectively. However, these task stages have been confounded with age group differences in learning performance that emerge later and to a lesser degree in older adults. To disentangle the effects of task stage from learning stage (i.e., when there is significant evidence of learning) on age group differences in the neural substrates of IAL, we acquired fMRI data while 28 younger (20.8 ± 2.3 years) and 22 older (73.6 ± 6.8 years) healthy adults completed the Triplets Learning Task, in which the location of two cues predicted the location of a target with high (HF) or low (LF) frequency. When matched for task stage, results revealed worse learning performance and increased IAL-related activity in the hippocampus during the early stage and in the globus pallidum during the late stage in older relative to younger adults. However, when matched for learning stage, there were no significant age group differences in learning performance or IAL-related activity. Thus, although learning emerges later for older adults, they are engaging similar brain regions as younger adults when learning the associations, suggesting that previous reports of age group differences reflect effects of age on task stage, but not learning stage.

Understanding Emotions: Origins and Roles of the Amygdala.

Emotions arise from activations of specialized neuronal populations in several parts of the cerebral cortex, notably the anterior cingulate, insula, ventromedial prefrontal, and subcortical structures, such as the amygdala, ventral striatum, putamen, caudate nucleus, and ventral tegmental area. Feelings are conscious, emotional experiences of these activations that contribute to neuronal networks mediating thoughts, language, and behavior, thus enhancing the ability to predict, learn, and reappraise stimuli and situations in the environment based on previous experiences. Contemporary theories of emotion converge around the key role of the amygdala as the central subcortical emotional brain structure that constantly evaluates and integrates a variety of sensory information from the surroundings and assigns them appropriate values of emotional dimensions, such as valence, intensity, and approachability. The amygdala participates in the regulation of autonomic and endocrine functions, decision-making and adaptations of instinctive and motivational behaviors to changes in the environment through implicit associative learning, changes in short- and long-term synaptic plasticity, and activation of the fight-or-flight response via efferent projections from its central nucleus to cortical and subcortical structures.

Pigeons acquire the 1-back task: Implications for implicit versus explicit learning?

In humans, a distinction can be made between implicit or procedural learning (involving stimulus-response associations) and explicit or declarative learning (involving verbalizable rules) that is relatively easy to make in verbal humans. According to several investigators, it is also possible to make such a distinction in nonverbal animals. One way is by training them on a conditional discrimination task (e.g., matching-to-sample) in which reinforcement for correct choice on the current trial is delayed until after a choice is made on the next trial - a method known as the 1-back procedure. According to Smith, Jackson, and Church ( Journal of Comparative Psychology, 134(4), 423-434, 2020), the delay between the sample-correct-comparison response on one trial and reinforcement obtained on the next trial is too long for implicit (associative) learning. Thus, according to this theory, learning must be explicit. In the present experiments we trained pigeons using the 1-back procedure. In Experiment 1, pigeons were trained on red/green 1-back matching using a non-correction procedure. Some of the pigeons showed significant learning. When a correction procedure was introduced, all the pigeons showed evidence of learning. In Experiment 2, new pigeons learned red/green 1-back matching with the correction procedure. In Experiment 3, new pigeons learned symbolic 1-back matching with yellow and blue conditional stimuli and red/green choice stimuli. Thus, pigeons can learn using 1-back reinforcement. Although it would appear that the pigeons acquired this task explicitly, we believe that this procedure does not adequately distinguish between implicit and explicit learning.

Implicit associative learning relates to basal ganglia gray matter microstructure in young and older adults

Older adults are impaired at implicit associative learning (IAL), or the learning of relationships between stimuli in the environment without conscious awareness. These age effects have been attributed to differential engagement of the basal ganglia (e.g. caudate, globus pallidus) and hippocampus throughout learning. However, no studies have examined gray matter diffusion relations with IAL, which can reveal microstructural properties that vary with age and contribute to learning. In this study, young (18–29 years) and older (65–87 years) adults completed the Triplet Learning Task, in which participants implicitly learn that the location of cues predict the target location on some trials (high frequency triplets). Diffusion imaging was also acquired and multicompartment diffusion metrics were calculated using neurite orientation dispersion and density imaging (NODDI). As expected, results revealed age deficits in IAL (smaller differences in performance to high versus low frequency triplets in the late learning stage) and age-related differences in basal ganglia and hippocampus free, hindered, and restricted diffusion. Significant correlations were seen between restricted caudate diffusion and early IAL and between hindered globus pallidus diffusion and late IAL, which were not moderated by age group. These findings indicate that individual differences in basal ganglia, but not hippocampal, gray matter microstructure contribute to learning, independent of age, further supporting basal ganglia involvement in IAL.

Associations between Attention and Implicit Associative Learning in Healthy Adults: The Role of Cortisol and Salivary Alpha-Amylase Responses to an Acute Stressor.

In this study, we investigated the associations between implicit associative learning with the cortisol and salivary alpha-amylase (sAA) stress response to an acute stressor as well as their associations with attention. Eighty one healthy adults (25 male) participated and either performed the socially evaluated cold-pressor test (SECPT) or a warm-water control task (WWT). Either prior to or immediately after the SECPT/WWT, participants implicitly learned digit-symbol pairs. A not-previously announced recall test was conducted about 20 min after the SECPT/WWT. Attention was assessed by means of a Stroop task at nine time points over the course of the experiment. Memory recall performance was not significantly associated with the acquisition time point (pre or post stressor) and did not significantly differ between the responder groups (i.e., non-responders, sAA-and-cortisol responders, only sAA responders, and only cortisol responders). Attentional performance increased throughout the experiment (i.e., reaction times in the Stroop task decreased). No differences in the attentional time course were found between the responder groups. However, some associations were found (puncorrected < 0.05) that did not pass the multiple comparison adjusted alpha level of αadjusted = 0.002, indicating different associations between attention and implicit learning between the responder groups. We conclude that the associations of sAA and cortisol responses with implicit learning are complex and are related to each other. Further studies in which both (sAA and cortisol responses) are selectively (de-) activated are needed. Furthermore, different learning tasks and less—potentially stressful—attentional assessments should be used in future research. Moreover, field studies are needed in which the associations between acute stress and implicit associative learning are investigated in everyday life.

Implicit acoustic sequence learning recruits the hippocampus.

The exclusive role of the medial temporal lobe in explicit memory has been questioned by several studies reporting medial temporal lobe involvement during implicit learning. Prior studies have demonstrated that hippocampal engagement is present during the implicit learning of perceptual associations, however, it is absent during learning response-related associations. Therefore, it was hypothesized that the function of the medial temporal lobe during implicit learning is related to the extraction of perceptual associations in general. While in most implicit learning tasks visual stimuli were used, the aim of the current functional magnetic resonance imaging (fMRI) study was to detect whether activations within medial temporal lobe structures are also found during implicit learning of auditory associations. In a modified version of the classical serial reaction time task, participants reacted to the presentation of five different tones. Unbeknownst to the participants, the tones were presented with an underlying sequential regularity that could be learned. To avoid an influence of response learning on acoustic associative learning, response buttons were remapped in every trial. After learning, two different tests were used to measure participants’ conscious knowledge about the underlying sequence in order to assess the amount of implicit memory and to exclude participants with explicit knowledge acquired during learning. fMRI results revealed hippocampal activations for implicit learning of the acoustic sequence. When detecting a relation between implicit learning of acoustic associations and hippocampal activations, this study indicated a relation between hippocampal activations and memory formation of perceptual-based relational representation regardless of explicit knowledge. Thus, present findings suggest a general functional role for the formation of sequenced perceptual associations independent of the involvement of awareness.

Implicit associative learning in synesthetes and nonsynesthetes.

Although cross-modal neural connections and genetic underpinnings are prominent in most current theories regarding the development of synesthesia, the potential role of associative learning in the formation of synesthetic associations has recently been revitalized. In this study, we investigated implicit associative learning in synesthetes and nonsynesthetes by recording reaction times to a target whose color was probabilistically correlated with its shape. A continuous measure of target detection at multiple time points during learning revealed that synesthetes and nonsynesthetes learn associations differently. Specifically, our results demonstrated a "fast-facilitation" learning effect for nonsynesthetes and a "fast-interference, slow-facilitation" learning effect for synesthetes. Additionally, synesthetes exhibited superior long-term memory for the learned associations in a surprise delayed retest. After this retest, participants implicitly learned new (shuffled) shape-color associations. We found that synesthetes experienced greater interference while learning these new shape-color associations. These results detail ways in which implicit associative learning and memory differ between synesthetes and nonsynesthetes.

A lab-controlled simulation of a letter–speech sound binding deficit in dyslexia

Dyslexic and non-dyslexic readers engaged in a short training aimed at learning eight basic letter–speech sound correspondences within an artificial orthography. We examined whether a letter–speech sound binding deficit is behaviorally detectable within the initial steps of learning a novel script. Both letter knowledge and word reading ability within the artificial script were assessed. An additional goal was to investigate the influence of instructional approach on the initial learning of letter–speech sound correspondences. We assigned children from both groups to one of three different training conditions: (a) explicit instruction, (b) implicit associative learning within a computer game environment, or (c) a combination of (a) and (b) in which explicit instruction is followed by implicit learning. Our results indicated that dyslexics were outperformed by the controls on a time-pressured binding task and a word reading task within the artificial orthography, providing empirical support for the view that a letter–speech sound binding deficit is a key factor in dyslexia. A combination of explicit instruction and implicit techniques proved to be a more powerful tool in the initial teaching of letter–sound correspondences than implicit training alone.

Does a simultaneous memory load affect older and younger adults’ implicit associative learning?

ABSTRACTThis study investigated the effects of a simultaneous memory load on implicit associative sequence learning using the Triplets Learning Task (TLT). Participants in the Simultaneous condition held a secondary task memory load during the TLT, while those in the Sequential condition also performed both tasks, but successively, rather than simultaneously. Thus, the Simultaneous condition had a memory load during the TLT, while the Sequential condition did not. Probe blocks without the secondary task allowed separation of effects on learning from effects on its expression. Results revealed that the simultaneous memory load affected older, but not younger adults, by suppressing the expression of learning, not learning itself. Thus, older and younger adults can learn probabilistic associations while holding a simultaneous memory load, but the load can limit the extent to which older adults adapt their performance to environmental structure. Results are consistent with theories which propose that implicit associative learning does not call on limited capacity resources, and highlight the importance of distinguishing effects of dual tasks on the expression of learning from those on learning itself.

No association of the BDNF val66met polymorphism with implicit associative vocabulary and motor learning.

Brain-derived neurotrophic factor (BDNF) has been suggested to play a major role in plasticity, neurogenesis and learning in the adult brain. The BDNF gene contains a common val66met polymorphism associated with decreased activity-dependent excretion of BDNF and a potential influence on behaviour, more specifically, on motor learning. The objective of this study was to determine the influence of the BDNF val66met polymorphism on short-term implicit associative learning and whether its influence is cognitive domain-specific (motor vs. language). A sample of 38 young healthy participants was genotyped, screened for background and neuropsychological differences, and tested with two associative implicit learning paradigms in two different cognitive domains, i.e., motor and vocabulary learning. Subjects performed the serial reaction time task (SRTT) to determine implicit motor learning and a recently established associative vocabulary learning task (AVL) for implicit learning of action and object words. To determine the influence of the BDNF polymorphism on domain-specific implicit learning, behavioural improvements in the two tasks were compared between val/val (n = 22) and met carriers (val/met: n = 15 and met/met: n = 1). There was no evidence for an impact of the BDNF val66met polymorphism on the behavioural outcome in implicit short-term learning paradigms in young healthy subjects. Whether this polymorphism plays a relevant role in long-term training paradigms or in subjects with impaired neuronal plasticity or reduced learning capacity, such as aged individuals, demented patients or patients with brain lesions, has to be determined in future studies.

The Effects of Aging on the Neural Basis of Implicit Associative Learning in a Probabilistic Triplets Learning Task

Few studies have investigated how aging influences the neural basis of implicit associative learning, and available evidence is inconclusive. One emerging behavioral pattern is that age differences increase with practice, perhaps reflecting the involvement of different brain regions with training. Many studies report hippocampal involvement early on with learning becoming increasingly dependent on the caudate with practice. We tested the hypothesis that the contribution of these regions to learning changes with age because of differential age-related declines in the striatum and hippocampi. We assessed age-related differences in brain activation during implicit associative learning using the Triplets Learning Task. Over three event-related fMRI runs, 11 younger and 12 healthy older adults responded to only the third (target) stimulus in sequences of three stimuli ("triplets") by corresponding key press. Unbeknown to participants, the first stimulus' location predicted one target location for 80% of trials and another target location for 20% of trials. Both age groups learned associative regularities but differences in favor of the younger adults emerged with practice. The neural basis of learning (response to predictability) was examined by identifying regions that showed a greater response to triplets that occurred more frequently. Both age groups recruited the hippocampus early, but with training, the younger adults recruited their caudate whereas the older adults continued to rely on their hippocampus. This pattern enables older adults to maintain near-young levels of performance early in training, but not later, and adds to evidence that implicit associative learning is supported by different brain networks in younger and older adults.

Constraints on Implicit Learning of Grammatical Form‐Meaning Connections

Although there is good evidence for implicit learning of associations between forms, little work has investigated implicit learning of form‐meaning connections, and the findings are somewhat contradictory. Two experiments were carried out using a novel reaction time methodology to investigate implicit learning of grammatical form‐meaning connections. Participants learned four novel articles but were not told about a critical semantic factor that determines agreement with the accompanying noun. Their task was to indicate as quickly as possible which of two pictures was being referred to by an article‐noun combination. The measure of learning was whether response times would slow down when the agreement rule was violated (i.e., when the wrong article was used for the picture being referred to). Experiment 1 revealed such an effect when articles correlated with noun animacy, even for participants with no reported awareness of this regularity. In Experiment 2 no such effect was obtained when the regularity concerned the relative size of two objects. It is concluded that grammatical form‐meaning connections may be learned implicitly, but learning is constrained by the nature of the meaning involved. It is argued that concepts are differentially available to implicit language learning processes.

Neurobehavioral correlates of the rapid formation of the symbolic control of visuospatial attention

Prior research suggests that nonpredictive symbolic central cues can produce nonvoluntary shifts of endogenous attention when associations between cues and spatial locations are overlearned during cognitive development. The present ERP study extends this research by first showing that overlearned cue-spatial location associations necessary to support nonvoluntary attentional orienting can be rapidly formed in adult humans. A second experiment indicates that the nonvoluntary orienting formed by such rapid learning is semireflexive (amenable to top-down influence) rather than reflexive (resistant to top-down influence). A third experiment suggests that the rapid formation of endogenous nonvoluntary orienting requires explicit rather than implicit learning of cue-location associations. These findings provide further support for a strong connection between neurocognitive representations of space, symbol meaning, and attentional control.

Implicit versus explicit associative learning and experimentally induced placebo hypoalgesia

The present study examined whether 1) placebo hypoalgesia can be generated through implicit associative learning (ie, conditioning in the absence of conscious awareness) and 2) the magnitude of placebo hypoalgesia changes when expectations about pain are made explicit. The temperature of heat pain stimuli was surreptitiously lowered during conditioning trials for the placebo cream and the magnitude of the placebo effect was assessed during a subsequent set of trials when the temperature was the same for both placebo and control conditions. To assess whether placebo hypoalgesia could be generated from an implicit tactile stimulus, a 2 × 2 design was used with direction of cream application as one factor and verbal information about which cream was being applied as the second factor. A significant placebo effect was observed when participants received verbal information about which cream was being applied but not following implicit conditioning alone. However, 87.5% of those who showed a placebo response as the result of implicit conditioning were able to accurately guess the order of cream application during the final trial, despite a lack of awareness about the sensory manipulation and low confidence in their ratings, suggesting implicit learning in some participants. In summary, implicit associative learning was evident in some participants but it was not sufficient to produce a placebo effect suggesting some level of explicit expectation or cognitive mediation may be necessary. Notably, the placebo response was abolished when expectations were made explicit, suggesting a delicate interplay between attention and expectation.

Implicit learning of social predictions

Humans exchange a range of nonverbal social signals in every interaction. It is an open question whether people use these signals, consciously or unconsciously, to guide social behavior. This experiment directly tested whether participants could learn to predict another person’s behavior using nonverbal cues in a single interaction, and whether explicit knowledge of the cue–outcome relationship was necessary for successful prediction. Participants played a computerized game of rock–paper–scissors against an avatar they believed was another participant. Sometimes the avatar generated a predictive facial cue before the play. On these trials, participants’ win-frequency increased over time, even if they did not acquire explicit knowledge of the predictive cue. The degree to which participants could predict the avatar (wins on cued trials) related to their self-reported liking of the avatar. These findings demonstrate the importance of implicit associative learning mechanisms in guiding social behavior on a moment-to-moment basis during interaction.

Patterns of Implicit Learning Below the Level of Conscious Knowledge

The objective of the present study was to evaluate patterns of implicit processing in a task where the acquisition of explicit and implicit knowledge occurs simultaneously. The number reduction task (NRT) was used as having two levels of organization, overt and covert, where the covert level of processing is associated with implicit associative and implicit procedural learning. One aim was to compare these two types of implicit processes in the NRT when sleep was or was not introduced between initial formation of task representations and subsequent NRT processing. To assess the effects of different sleep stages, two sleep groups (early- and late-night groups) were used where initial training of the task was separated from subsequent retest by 3 h full of predominantly slow wave sleep (SWS) or rapid eye movement (REM) sleep. In two no-sleep groups, no interval was introduced between initial and subsequent NRT performance. A second aim was to evaluate the interaction between procedural and associative implicit learning in the NRT. Implicit associative learning was measured by the difference between the speed of responses that could or could not be predicted by the covert abstract regularity of the task. Implicit procedural on-line learning was measured by the practice-based increased speed of performance with time on task. Major results indicated that late-night sleep produced a substantial facilitation of implicit associations without modifying individual ability for explicit knowledge generation or for procedural on-line learning. This was evidenced by the higher rate of subjects who gained implicit knowledge of abstract task structure in the late-night group relative to the early-night and no-sleep groups. Independently of sleep, gain of implicit associative knowledge was accompanied by a relative slowing of responses to unpredictable items suggesting reciprocal interactions between associative and motor procedural processes within the implicit system. These observations provide evidence for the separability and interactions of different patterns of processing within implicit memory.

Not What You Expect: Experience but not Expectancy Predicts Conditioned Responses in Human Visual and Supplementary Cortex

When paired with aversive events, visual conditioned stimuli (CS) provoke increased activations in visual cortex. It is unclear however whether these changes reflect cognitive processes such as expectancy of the aversive unconditioned stimulus (US), or implicit associative learning of the contingencies outside awareness. Here, we used the "gambler's fallacy" phenomenon to parametrically and inversely manipulate the expectancy of an US and the number of conditioning trials: Increasing the number of CS-US pairings was associated with participants expecting the US to be less likely and vice versa. Magnetocortical activity evoked by the CS in occipital and supplementary motor areas was linearly related to the associative strength (number of CS-US pairings), but decreased as a function of expectancy. These results suggest that the cortical facilitation of fear cue processing is determined by associative strength and previous exposure to learning contingencies rather than by the cognitive anticipation for the US.

AGL StimSelect: Software for automated selection of stimuli for artificial grammar learning

Artificial grammar learning (AGL) is an experimental paradigm that has been used extensively incognitive research for many years to study implicit learning, associative learning, and generalization on the basis of either similarity or rules. Without computer assistance, it is virtually impossible to generate appropriate grammatical training stimuli along with grammatical or nongrammatical test stimuli that control relevant psychological variables. We present the first flexible, fully automated software for selecting AGL stimuli. The software allows users to specify a grammar of interest, and to manipulate characteristics of training and test sequences, and their relationship to each other. The user therefore has direct control over stimulus features that may influence learning and generalization in AGL tasks. The software, AGL StimSelect, enables researchers to develop AGL designs that would not be feasible without automatic stimulus selection. It is implemented in MATLAB.