Shawn W. Ell

FROST: A Distributed Neurocomputational Model of Working Memory Maintenance

Many studies suggest that the sustained activation underlying working memory (WM) maintenance is mediated by a distributed network that includes the prefrontal cortex and other structures (e.g., posterior parietal cortex, thalamus, globus pallidus, and the caudate nucleus). A computational model of WM, called FROST (short for FROntal-Striatal-Thalamic), is proposed in which the representation of items and spatial positions is encoded in the lateral prefrontal cortex. During delay intervals, activation in these prefrontal cells is sustained via parallel, prefrontal cortical-thalamic loops. Activation reverberates in these loops because prefrontal cortical excitation of the head of the caudate nucleus leads to disinhibition of the thalamus (via the globus pallidus). FROST successfully accounts for a wide variety of WM data, including single-cell recording data and human behavioral data.

Focal putamen lesions impair learning in rule-based, but not information-integration categorization tasks.

Previous research on the role of the basal ganglia in category learning has focused on patients with Parkinsons and Huntingtons disease, neurodegenerative diseases frequently accompanied by additional cortical pathology. The goal of the present study was to extend this work to patients with basal ganglia lesions due to stroke, asking if similar changes in performance would be observed in patients with more focal pathology. Patients with basal ganglia lesions centered in the putamen (6 left side, 1 right side) were tested on rule-based and information-integration visual categorization tasks. In rule-based tasks, it is assumed that participants can learn the category structures through an explicit reasoning process. In information-integration tasks, optimal performance requires the integration of information from two or more stimulus components, and participants are typically unaware of the category rules. Consistent with previous studies involving patients with degenerative disorders of the basal ganglia, the stroke patients were impaired on the rule-based task, and quantitative, model-based analyses indicate that this deficit was due to the inefficient application of decision strategies. In contrast, the patients were unimpaired on the information-integration task. This pattern of results provides converging evidence supporting a role of the basal ganglia and, in particular, the putamen in rule-based category learning.

Learning robust cortico-cortical associations with the basal ganglia: An integrative review

This article focuses on the interaction between the basal ganglia (BG) and prefrontal cortex (PFC). The BG are a group of nuclei at the base of the forebrain that are highly connected with cortex. A century of research suggests that the role of the BG is not exclusively motor, and that the BG also play an important role in learning and memory. In this review article, we argue that one important role of the BG is to train connections between posterior cortical areas and frontal cortical regions that are responsible for automatic behavior after extensive training. According to this view, one effect of BG trial-and-error learning is to activate the correct frontal areas shortly after posterior associative cortex activation, thus allowing for Hebbian learning of robust, fast, and efficient cortico-cortical processing. This hypothesized process is general, and the content of the learned associations depends on the specific areas involved (e.g., associations involving premotor areas would be more closely related to behavior than associations involving the PFC). We review experiments aimed at pinpointing the function of the BG and the frontal cortex and show that these results are consistent with the view that the BG is a general purpose trainer for cortico-cortical connections. We conclude with a discussion of some implications of the integrative framework and how this can help better understand the role of the BG in many different tasks.

Prefrontal contributions to rule-based and information-integration category learning.

Previous research revealed that the basal ganglia play a critical role in category learning [Ell, S. W., Marchant, N. L., & Ivry, R. B. (2006). Focal putamen lesions impair learning in rule-based, but not information-integration categorization tasks. Neuropsychologia, 44(10), 1737-1751; Maddox, W. T. & Filoteo, J. V. (2007). Modeling visual attention and category learning in amnesiacs, striatal-damaged patients and normal aging. In Advances in Clinical-cognitive science: formal modeling and assessment of processes and symptoms (pp. 113-146). Washington DC: American Psychological Association] but less is known about the specific role of prefrontal cortical (PFC) regions in category learning. The current study examined rule-based (RB) and information-integration (II) category learning in 13 patients with damage primarily to ventral PFC regions. After 600 learning trials with feedback, patients were significantly less accurate than matched controls on both RB and II learning. Model-based analysis identified subgroups of patients whose impaired performance in each task was due to the use of sub-optimal learning strategies. Those patients impaired at either II or RB learning, performed significantly worse on the Wisconsin Card Sorting Test, a test of abstract rule formation and the ability to shift and maintain rules. Lesion analysis pointed to damage in a fairly circumscribed region of ventral medial prefrontal cortex as common to the impaired group of patients and those patients without ventral PFC damage mostly performed normally. These results provide further evidence that the ventromedial prefrontal cortex is critically important for the ability to monitor and integrate feedback in order to select and maintain optimal learning strategies.

The effects of category overlap on information-integration and rule-based category learning

In three experiments, we investigated whether the amount of category overlap constrains the decision strategies used in category learning, and whether such constraints depend on the type of category structures used. Experiments 1 and 2 used a category-learning task requiring perceptual integration of information from multiple dimensions (an information-integration task) and Experiment 3 used a task requiring the application of an explicit strategy (a rule-based task). In the information-integration task, participants used perceptual-integration strategies at moderate levels of category overlap, but explicit strategies at extreme levels of overlap—even when such strategies were suboptimal. In contrast, in the rule-based task, participants used explicit strategies, regardless of the level of category overlap. These data are consistent with a multiple systems view of category learning, and suggest that categorization strategy depends on the type of task that is used, and on the degree to which each stimulus is probabilistically associated with the contrasting categories.

Criterial noise effects on rule-based category learning: the impact of delayed feedback.

Variability in the representation of the decision criterion is assumed in many category-learning models, yet few studies have directly examined its impact. On each trial, criterial noise should result in drift in the criterion and will negatively impact categorization accuracy, particularly in rule-based categorization tasks, where learning depends on the maintenance and manipulation of decision criteria. In three experiments, we tested this hypothesis and examined the impact of working memory on slowing the drift rate. In Experiment 1, we examined the effect of drift by inserting a 5-sec delay between the categorization response and the delivery of corrective feedback, and working memory demand was manipulated by varying the number of decision criteria to be learned. Delayed feedback adversely affected performance, but only when working memory demand was high. In Experiment 2, we built on a classic finding in the absolute identification literature and demonstrated that distributing the criteria across multiple dimensions decreases the impact of drift during the delay. In Experiment 3, we confirmed that the effect of drift during the delay is moderated by working memory. These results provide important insights into the interplay between criterial noise and working memory, as well as providing important constraints for models of rule-based category learning.

Rule-Based Categorization Deficits in Focal Basal Ganglia Lesion and Parkinson’s Disease Patients

Patients with basal ganglia (BG) pathology are consistently found to be impaired on rule-based category learning tasks in which learning is thought to depend upon the use of an explicit, hypothesis-guided strategy. The factors that influence this impairment remain unclear. Moreover, it remains unknown if the impairments observed in patients with degenerative disorders such as Parkinsons disease (PD) are also observed in those with focal BG lesions. In the present study, we tested patients with either focal BG lesions or PD on two categorization tasks that varied in terms of their demands on selective attention and working memory. Individuals with focal BG lesions were impaired on the task in which working memory demand was high and performed similarly to healthy controls on the task in which selective-attention demand was high. In contrast, individuals with PD were impaired on both tasks, and accuracy rates did not differ between on and off medication states for a subset of patients who were also tested after abstaining from dopaminergic medication. Quantitative, model-based analyses attributed the performance deficit for both groups in the task with high working memory demand to the utilization of suboptimal strategies, whereas the PD-specific impairment on the task with high selective-attention demand was driven by the inconsistent use of an optimal strategy. These data suggest that the demands on selective attention and working memory affect the presence of impairment in patients with focal BG lesions and the nature of the impairment in patients with PD.

When bad stress goes good: increased threat reactivity predicts improved category learning performance

The way in which we respond to everyday stressors can have a profound impact on cognitive functioning. Maladaptive stress responses in particular are generally associated with impaired cognitive performance. We argue, however, that the cognitive system mediating task performance is also a critical determinant of the stress-cognition relationship. Consistent with this prediction, we observed that stress reactivity consistent with a maladaptive, threat response differentially predicted performance on two categorization tasks. Increased threat reactivity predicted enhanced performance on an information-integration task (i.e., learning is thought to depend upon a procedural-based memory system), and a (nonsignificant) trend for impaired performance on a rule-based task (i.e., learning is thought to depend upon a hypothesis-testing system). These data suggest that it is critical to consider both variability in the stress response and variability in the cognitive system mediating task performance in order to fully understand the stress-cognition relationship.

The impact of category separation on unsupervised categorization

Most previous research on unsupervised categorization has used unconstrained tasks in which no instructions are provided about the underlying category structure or in which the stimuli are not clustered into categories. Few studies have investigated constrained tasks in which the goal is to learn predefined stimulus clusters in the absence of feedback. These studies have generally reported good performance when the stimulus clusters could be separated by a one-dimensional rule. In the present study, we investigated the limits of this ability. Results suggest that even when two stimulus clusters are as widely separated, as in previous studies, performance is poor if within-category variance on the relevant dimension is nonnegligible. In fact, under these conditions, many participants failed even to identify the single relevant stimulus dimension. This poor performance is generally incompatible with all current models of unsupervised category learning.

Unsupervised category learning with integral-dimension stimuli

Despite the recent surge in research on unsupervised category learning, the majority of studies have focused on unconstrained tasks in which no instructions are provided about the underlying category structure. Relatively little research has focused on constrained tasks in which the goal is to learn predefined stimulus clusters in the absence of feedback. The few studies that have addressed this issue have focused almost exclusively on stimuli for which it is relatively easy to attend selectively to the component dimensions (i.e., separable dimensions). In the present study, we investigated the ability of participants to learn categories constructed from stimuli for which it is difficult, if not impossible, to attend selectively to the component dimensions (i.e., integral dimensions). The experiments demonstrate that individuals are capable of learning categories constructed from the integral dimensions of brightness and saturation, but this ability is generally limited to category structures requiring selective attention to brightness. As might be expected with integral dimensions, participants were often able to integrate brightness and saturation information in the absence of feedback—an ability not observed in previous studies with separable dimensions. Even so, there was a bias to weight brightness more heavily than saturation in the categorization process, suggesting a weak form of selective attention to brightness. These data present an important challenge for the development of models of unsupervised category learning.