Daphné Coomans

Freezing of gait in Parkinson's disease: disturbances in automaticity and control

Recent studies emphasize a key role of controlled operations, such as set-shifting and inhibition, in the occurrence of freezing of gait (FOG) in Parkinsons disease (PD). However, FOG can also be characterized as a de-automatization disorder, showing impairments in both the execution and acquisition of automaticity. The observed deficits in automaticity and executive functioning indicate that both processes are malfunctioning in freezers. Therefore, to explain FOG from a cognitive-based perspective, we present a model describing the pathways involved in automatic and controlled processes prior to a FOG episode. Crucially, we focus on disturbances in automaticity and control, regulated by the frontostriatal circuitry. In complex situations, non-freezing PD patients may compensate for deficits in automaticity by switching to increased cognitive control. However, as both automatic and controlled processes are more severely impaired in freezers, this hampers cognitive compensation in FOG, resulting in a potential breakdown. Future directions for cognitive rehabilitation are proposed, based on the cognitive model we put forward.

Impaired implicit sequence learning in Parkinson's disease patients with freezing of gait.

OBJECTIVE Freezing of gait (FOG) in Parkinsons disease (PD) may involve specific impairments in acquiring automaticity under working memory load. This study examined whether implicit sequence learning, with or without a secondary task, is impaired in patients with FOG. METHOD Fourteen freezers (FRs), 14 nonfreezers (nFRs), and 14 matched healthy controls (HCs) performed a serial reaction time (SRT) task with a deterministic stimulus sequence under single-task (ST) and dual-task (DT) conditions. The increase in reaction times (RTs) for random compared with sequenced blocks was used as a measure of implicit sequence learning. Neuropsychological tests assessing global cognitive functioning and executive dysfunction were administered in order to investigate their relation to sequence learning. RESULTS nFRs and HCs showed significant implicit sequence learning effects (p < 0.001). FRs demonstrated a tendency to learn sequence-specific information in the SRT-ST task (p = 0.07) but not in the SRT-DT task (p = 0.69). Severity of FOG, however, correlated positively with SRT-DT task performance (r = -0.56; p < 0.05). CONCLUSIONS The present results suggest that PD patients suffering from FOG pathology exhibit a specific impairment in the acquisition of automaticity. When working memory capacity is supplementarily loaded by adding a DT, sequence learning in FRs becomes increasingly impaired. These findings indicate that therapies should focus on extensive training in acquiring novel motor activities and reducing working memory load to improve learning in FOG.

Intact first- and second-order implicit sequence learning in secondary-school-aged children with developmental dyslexia

We examined the influence of task complexity on implicit sequence learning in secondary-school-aged children with developmental dyslexia (DD). This was done to determine whether automatization problems in reading extend to the automatization of all skill and depend on the complexity of the to-be-learned skill. A total of 28 dyslexic children between 12 and 15 years and 28 matched control children carried out two serial reaction time tasks using a first-order conditional (FOC) and second-order conditional (SOC) sequence. In both tasks, children incidentally learned a sequence of hidden target positions, but whereas FOC sequence learning could be based on knowledge about the immediate preceding position, SOC sequence learning required more complex knowledge about the previous two positions. The results demonstrated that sequence learning was highly comparable in dyslexic and control children, regardless of the sequence complexity. This shows that implicit sequence learning, as manifested in the present study, is maintained in DD and is unrelated to task complexity. We suggest that previous reports of sequence-learning deficits in DD can be accounted for by attenuated explicit sequence learning, possibly related to malfunctions in prefrontal processing. The present findings indicate that deficits in skill learning and automatization in DD are not general in nature, but task dependent.

Cognitive control: A role for implicit learning?

We investigated the influence of implicit learning on cognitive control. In a sequential Stroop task, participants implicitly learned a sequence placed on the color of the Stroop words. In Experiment 1, Stroop conflict was lower in sequenced than in random trials (learning-improved control). However, as these results were derived from an interaction between learning and conflict, they could also be explained by improved implicit learning (difference between random and sequenced trials), under incongruent compared with congruent trials (control-improved learning). Therefore, we further unraveled the direction of the interaction in 2 additional experiments. In Experiment 2, participants who learned the color sequence were no better at resolving conflict than participants who did not undergo sequence training. This shows that implicit knowledge does not directly reduce conflict (no learning-improved control). In Experiment 3, the amount of conflict did not directly improve learning either (no control-improved learning). However, conflict had a significant impact on the expression of implicit learning, as most knowledge was expressed under the highest amount of conflict. Thus, task-optimization was accomplished by an increased reliance on implicit sequence knowledge under high conflict. These findings demonstrate that implicit learning processes can be flexibly recruited to support cognitive control functions.

Perceptual Load Improves the Expression but not Learning of Relevant Sequence Information

In two experiments, we investigated the hypothesis of Rowland and Shanks (2006a) that sequence learning of relevant information is resistant to variations in perceptual load. Under conditions of increased selection difficulty, participants incidentally learned a sequence of targets presented together with three distractors. Target and distractors were composed of pairs of letters and shared more or less features with each other, rendering perceptual identification of the target either more (high load) or less (low load) attention demanding. The expression of sequence learning improved significantly under high load conditions as compared to low load conditions. This could indicate that the cognitive system promotes the development of response-based sequence learning in order to cope with the attentional demands arising from high perceptual load. However, the learning process proved to be unaffected by perceptual load when tested under baseline conditions without distractors (Experiment 1) or under opposite load conditions as during training (Experiment 2). This demonstrates that sequence learning is not influenced by increasing selection demands and suggests that sequence learning runs independently of input attention.

On the automaticity of pure perceptual sequence learning.

We investigated the automaticity of implicit sequence learning by varying perceptual load in a pure perceptual sequence learning paradigm. Participants responded to the randomly changing identity of a target, while the irrelevant target location was structured. In Experiment 1, the target was presented under low or high perceptual load during training, whereas testing occurred without load. Unexpectedly, no sequence learning was observed. In Experiment 2, perceptual load was introduced during the test phase to determine whether load is required to express perceptual knowledge. Learning itself was unaffected by visuospatial demands, but more learning was expressed under high load test conditions. In Experiment 3, we demonstrated that perceptual load is not required for the acquisition of perceptual sequence knowledge. These findings suggest that perceptual load does not mediate the perceptual sequence learning process itself, supporting the automaticity of implicit learning, but is mandatory for the expression of pure perceptual sequence knowledge.

The effect of cognitive aging on implicit sequence learning and dual tasking

We investigated the influence of attentional demands on sequence-specific learning by means of the serial reaction time task (Nissen and Bullemer, 1987) in young (age 18–25) and aged (age 55–75) adults. Participants had to respond as fast as possible to a stimulus presented in one of four horizontal locations by pressing a key corresponding to the spatial position of the stimulus. During the training phase sequential blocks were accompanied by (1) no secondary task (single), (2) a secondary tone counting task (dual tone), or (3) a secondary shape counting task (dual shape). Both secondary tasks were administered to investigate whether low and high interference tasks interact with implicit learning and age. The testing phase, under baseline single condition, was implemented to assess differences in sequence-specific learning between young and aged adults. Results indicate that (1) aged subjects show less sequence learning compared to young adults, (2) young participants show similar implicit learning effects under both single and dual task conditions when we account for explicit awareness, and (3) aged adults demonstrate reduced learning when the primary task is accompanied with a secondary task, even when explicit awareness is included as a covariate in the analysis. These findings point to implicit learning deficits under dual task conditions that can be related to cognitive aging, demonstrating the need for sufficient cognitive resources while performing a sequence learning task.

Target–flanker discriminability affects conflict size but not sustained suppression

On successive trials, repetitions of irrelevant information often tend to reduce congruency effects as compared to alternations of irrelevant information. The preferred explanation for this congruency modulation is the sustained-suppression hypothesis, suggesting that suppression of the irrelevant information on a given trial perseveres into the subsequent trial. However, in contrast to the generality of this idea, this modulation is only stable when the irrelevant information contains spatial features, which coincided in the existing research with large conflict sizes and response conflicts. In two arrow flanker experiments, we investigated whether the congruency modulation depends on the size of the conflict, by manipulating the saliency of the target (Experiment 1) and the flankers (Experiment 2). Although these manipulations affected the size of the conflict caused by the flankers, neither experiment showed an influence of conflict size on the reduction of the congruency effect for repetitions as compared to alternation of the irrelevant flankers. We conclude that sustained-suppression is not a consequence of large conflicts, at least if sustained-suppression causes the congruency modulation.

The effect of attentional load on implicit sequence learning in children and young adults

We investigated the effect of a secondary task on implicit sequence learning in children and young adults. A serial reaction time (SRT) task was administered to 8-to-10 year old children and 18-to-22 year old adults. Participants reacted to the location of a target presented in one of four locations on the screen with a spatially corresponding response key. Unknown to participants, the location at which the target appeared was structured according to a deterministic sequence. Occasionally, the black target dot was replaced by a red target dog. To assess the effect of attentional load on implicit sequence learning, half of the participants of each age group was assigned to the single task condition, while the other half executed the task under dual task conditions. Whereas participants in the single task condition could ignore the change in target identity, dual task participants additionally had to count the number of times the black dot was replaced by a red dog to increase the attentional load. Sequence learning was tested under single task conditions in both conditions. Z-transformed results indicate that young adults generally showed more sequence learning than children. Importantly, the secondary task had no effect on sequence learning in children, since children learned as much under dual task conditions as under single task conditions. Adults, on the other hand, showed a different result pattern, as they displayed more sequence learning under single task than under dual task conditions. We surmise that this result is due to the vainly attempt of adults, but not children, to integrate both sequences.

Is sequence awareness mandatory for perceptual sequence learning: An assessment using a pure perceptual sequence learning design

We examined the role of sequence awareness in a pure perceptual sequence learning design. Participants had to react to the targets colour that changed according to a perceptual sequence. By varying the mapping of the targets colour onto the response keys, motor responses changed randomly. The effect of sequence awareness on perceptual sequence learning was determined by manipulating the learning instructions (explicit versus implicit) and assessing the amount of sequence awareness after the experiment. In the explicit instruction condition (n = 15), participants were instructed to intentionally search for the colour sequence, whereas in the implicit instruction condition (n = 15), they were left uninformed about the sequenced nature of the task. Sequence awareness after the sequence learning task was tested by means of a questionnaire and the process-dissociation-procedure. The results showed that the instruction manipulation had no effect on the amount of perceptual sequence learning. Based on their report to have actively applied their sequence knowledge during the experiment, participants were subsequently regrouped in a sequence strategy group (n = 14, of which 4 participants from the implicit instruction condition and 10 participants from the explicit instruction condition) and a no-sequence strategy group (n = 16, of which 11 participants from the implicit instruction condition and 5 participants from the explicit instruction condition). Only participants of the sequence strategy group showed reliable perceptual sequence learning and sequence awareness. These results indicate that perceptual sequence learning depends upon the continuous employment of strategic cognitive control processes on sequence knowledge. Sequence awareness is suggested to be a necessary but not sufficient condition for perceptual learning to take place.