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Research paper thumbnail of Hierarchical control of procedural and declarative category-learning systems

NeuroImage, Jan 15, 2017

Substantial evidence suggests that human category learning is governed by the interaction of mult... more Substantial evidence suggests that human category learning is governed by the interaction of multiple qualitatively distinct neural systems. In this view, procedural memory is used to learn stimulus-response associations, and declarative memory is used to apply explicit rules and test hypotheses about category membership. However, much less is known about the interaction between these systems: how is control passed between systems as they interact to influence motor resources? Here, we used fMRI to elucidate the neural correlates of switching between procedural and declarative categorization systems. We identified a key region of the cerebellum (left Crus I) whose activity was bidirectionally modulated depending on switch direction. We also identified regions of the default mode network (DMN) that were selectively connected to left Crus I during switching. We propose that the cerebellum-in coordination with the DMN-serves a critical role in passing control between procedural and dec...

Research paper thumbnail of Context-dependent savings in procedural category learning

Brain and Cognition, 2014

Environmental context can have a profound influence on the efficacy of intervention protocols des... more Environmental context can have a profound influence on the efficacy of intervention protocols designed to eliminate undesirable behaviors. This is clearly seen in drug rehabilitation clinics where patients often relapse soon after leaving the context of the treatment facility. A similar pattern is commonly observed in controlled laboratory studies of context-dependent savings in instrumental conditioning, where simply placing an animal back into the original conditioning chamber can renew an extinguished instrumental response. Surprisingly, context-dependent savings in human procedural learning has not been carefully examined in the laboratory. Here, we provide the first known empirical demonstration of context-dependent savings in a perceptual categorization task known to recruit procedural learning. We also present a computational account of these savings using a biologically detailed model in which a key role is played by cholinergic interneurons in the striatum.

Research paper thumbnail of The neurobiology of categorization

The Making of Human Concepts, 2010

Research paper thumbnail of Implicit and explicit category learning by macaques (Macaca mulatta) and humans (Homo sapiens)

Journal of Experimental Psychology: Animal Behavior Processes, 2010

An influential theoretical perspective differentiates in humans an explicit, rule-based system of... more An influential theoretical perspective differentiates in humans an explicit, rule-based system of category learning from an implicit system that slowly associates different regions of perceptual space with different response outputs. This perspective was extended for the 1st time to the category learning of nonhuman primates. Humans (Homo sapiens) and macaques (Macaca mulatta) learned categories composed of sine-wave gratings that varied across trials in bar width and bar orientation. The categories had either a single-dimensional, rule-based solution or a two-dimensional, information-integration solution. Humans strongly dimensionalized the stimuli and learned the rule-based task far more quickly. Six macaques showed the same performance advantage in the rule-based task. In humans, rule-based category learning is linked to explicit cognition, consciousness, and declarative reports about the contents of cognition. These results demonstrate an empirical continuity between human and nonhuman primate cognition, suggesting that nonhuman primates may have some structural components of humans' capacity for explicit cognition.

Research paper thumbnail of Implicit and explicit category learning by capuchin monkeys (Cebus apella)

Journal of Comparative Psychology, 2012

Current theories of human categorization differentiate an explicit, rule-based system of category... more Current theories of human categorization differentiate an explicit, rule-based system of category learning from an implicit system that slowly associates regions of perceptual space with response outputs. The researchers extended this theoretical differentiation to the category learning of New World primates. Four capuchins (Cebus apella) learned categories of circular sine-wave gratings that varied in bar spatial frequency and orientation. The rule-based and information-integration tasks, respectively, had onedimensional and two-dimensional solutions. Capuchins, like humans, strongly dimensionalized the stimuli and learned the rule-based task more easily. The results strengthen the suggestion that nonhuman primates have some structural components of humans' capacity for explicit categorization, which in humans is linked to declarative cognition and consciousness. The results also strengthen the primate contrast to other vertebrate species that may lack the explicit system. Therefore, the results raise important questions about the origins of the explicit categorization system during cognitive evolution and about its overall phylogenetic distribution.

Research paper thumbnail of A Computational Model of How Cholinergic Interneurons Protect Striatal-dependent Learning

Journal of Cognitive Neuroscience, 2011

An essential component of skill acquisition is learning the environmental conditions in which tha... more An essential component of skill acquisition is learning the environmental conditions in which that skill is relevant. This article proposes and tests a neurobiologically detailed theory of how such learning is mediated. The theory assumes that a key component of this learning is provided by the cholinergic interneurons in the striatum known as tonically active neurons (TANs). The TANs are assumed to exert a tonic inhibitory influence over cortical inputs to the striatum that prevents the execution of any striatal-dependent actions. The TANs learn to pause in rewarding environments, and this pause releases the striatal output neurons from this inhibitory effect, thereby facilitating the learning and expression of striatal-dependent behaviors. When rewards are no longer available, the TANs cease to pause, which protects striatal learning from decay. A computational version of this theory accounts for a variety of single-cell recording data and some classic behavioral phenomena, includ...

Research paper thumbnail of Decision letter: Motor memories of object dynamics are categorically organized

The ability to predict the dynamics of objects, linking applied force to motion, underlies our ca... more The ability to predict the dynamics of objects, linking applied force to motion, underlies our capacity to perform many of the tasks we carry out on a daily basis. Thus, a fundamental question is how the dynamics of the myriad objects we interact with are organized in memory. Using a custom-built three-dimensional robotic interface that allowed us to simulate objects of varying appearance and weight, we examined how participants learned the weights of sets of objects that they repeatedly lifted. We find strong support for the novel hypothesis that motor memories of object dynamics are organized categorically, in terms of families, based on covariation in their visual and mechanical properties. A striking prediction of this hypothesis, supported by our findings and not predicted by standard associative map models, is that outlier objects with weights that deviate from the family-predicted weight will never be learned despite causing repeated lifting errors. Editor's evaluation This paper provides compelling evidence from several behavioural experiments that recently learned estimates of the mass of novel objects possess a categorical structure in memory. It further links this categorical structure to important aspects of motor control, and provides a compelling window through which to consider the role of multiple systems in the learning and memory of novel object dynamics.

Research paper thumbnail of Declarative strategies persist under increased cognitive load

Psychonomic Bulletin & Review, 2015

When humans simultaneously execute multiple tasks, performance on individual tasks suffers. Compl... more When humans simultaneously execute multiple tasks, performance on individual tasks suffers. Complementing existing theories, this article poses a novel question to investigate interactions between memory systems supporting multi-tasking performance: When a primary and dual task both recruit declarative learning and memory systems, does simultaneous performance of both tasks impair primary task performance because learning in the declarative system is reduced, or because control of the primary task is passed to slower procedural systems? To address this question, participants were trained on either a perceptual categorization task believed to rely on procedural learning or one of three different categorization tasks believed to rely on declarative learning. Task performance was examined with and without a simultaneous dual task thought to recruit working memory and executive attention. To test whether the categories were learned procedurally or declaratively, the response keys were switched after a learning criterion had been reached. Large impairments in performance after switching the response keys are taken to indicate procedural learning, and small impairments are taken to indicate Electronic supplementary material The online version of this article (declarative learning. Our results suggest that the declarative memory categorization tasks (regardless of task difficulty) were learned by declarative systems, regardless of whether they were learned under dual-task conditions.

Research paper thumbnail of Hierarchical control of procedural and declarative category-learning systems

NeuroImage, Jan 15, 2017

Substantial evidence suggests that human category learning is governed by the interaction of mult... more Substantial evidence suggests that human category learning is governed by the interaction of multiple qualitatively distinct neural systems. In this view, procedural memory is used to learn stimulus-response associations, and declarative memory is used to apply explicit rules and test hypotheses about category membership. However, much less is known about the interaction between these systems: how is control passed between systems as they interact to influence motor resources? Here, we used fMRI to elucidate the neural correlates of switching between procedural and declarative categorization systems. We identified a key region of the cerebellum (left Crus I) whose activity was bidirectionally modulated depending on switch direction. We also identified regions of the default mode network (DMN) that were selectively connected to left Crus I during switching. We propose that the cerebellum-in coordination with the DMN-serves a critical role in passing control between procedural and dec...

Research paper thumbnail of Context-dependent savings in procedural category learning

Brain and Cognition, 2014

Environmental context can have a profound influence on the efficacy of intervention protocols des... more Environmental context can have a profound influence on the efficacy of intervention protocols designed to eliminate undesirable behaviors. This is clearly seen in drug rehabilitation clinics where patients often relapse soon after leaving the context of the treatment facility. A similar pattern is commonly observed in controlled laboratory studies of context-dependent savings in instrumental conditioning, where simply placing an animal back into the original conditioning chamber can renew an extinguished instrumental response. Surprisingly, context-dependent savings in human procedural learning has not been carefully examined in the laboratory. Here, we provide the first known empirical demonstration of context-dependent savings in a perceptual categorization task known to recruit procedural learning. We also present a computational account of these savings using a biologically detailed model in which a key role is played by cholinergic interneurons in the striatum.

Research paper thumbnail of The neurobiology of categorization

The Making of Human Concepts, 2010

Research paper thumbnail of Implicit and explicit category learning by macaques (Macaca mulatta) and humans (Homo sapiens)

Journal of Experimental Psychology: Animal Behavior Processes, 2010

An influential theoretical perspective differentiates in humans an explicit, rule-based system of... more An influential theoretical perspective differentiates in humans an explicit, rule-based system of category learning from an implicit system that slowly associates different regions of perceptual space with different response outputs. This perspective was extended for the 1st time to the category learning of nonhuman primates. Humans (Homo sapiens) and macaques (Macaca mulatta) learned categories composed of sine-wave gratings that varied across trials in bar width and bar orientation. The categories had either a single-dimensional, rule-based solution or a two-dimensional, information-integration solution. Humans strongly dimensionalized the stimuli and learned the rule-based task far more quickly. Six macaques showed the same performance advantage in the rule-based task. In humans, rule-based category learning is linked to explicit cognition, consciousness, and declarative reports about the contents of cognition. These results demonstrate an empirical continuity between human and nonhuman primate cognition, suggesting that nonhuman primates may have some structural components of humans' capacity for explicit cognition.

Research paper thumbnail of Implicit and explicit category learning by capuchin monkeys (Cebus apella)

Journal of Comparative Psychology, 2012

Current theories of human categorization differentiate an explicit, rule-based system of category... more Current theories of human categorization differentiate an explicit, rule-based system of category learning from an implicit system that slowly associates regions of perceptual space with response outputs. The researchers extended this theoretical differentiation to the category learning of New World primates. Four capuchins (Cebus apella) learned categories of circular sine-wave gratings that varied in bar spatial frequency and orientation. The rule-based and information-integration tasks, respectively, had onedimensional and two-dimensional solutions. Capuchins, like humans, strongly dimensionalized the stimuli and learned the rule-based task more easily. The results strengthen the suggestion that nonhuman primates have some structural components of humans' capacity for explicit categorization, which in humans is linked to declarative cognition and consciousness. The results also strengthen the primate contrast to other vertebrate species that may lack the explicit system. Therefore, the results raise important questions about the origins of the explicit categorization system during cognitive evolution and about its overall phylogenetic distribution.

Research paper thumbnail of A Computational Model of How Cholinergic Interneurons Protect Striatal-dependent Learning

Journal of Cognitive Neuroscience, 2011

An essential component of skill acquisition is learning the environmental conditions in which tha... more An essential component of skill acquisition is learning the environmental conditions in which that skill is relevant. This article proposes and tests a neurobiologically detailed theory of how such learning is mediated. The theory assumes that a key component of this learning is provided by the cholinergic interneurons in the striatum known as tonically active neurons (TANs). The TANs are assumed to exert a tonic inhibitory influence over cortical inputs to the striatum that prevents the execution of any striatal-dependent actions. The TANs learn to pause in rewarding environments, and this pause releases the striatal output neurons from this inhibitory effect, thereby facilitating the learning and expression of striatal-dependent behaviors. When rewards are no longer available, the TANs cease to pause, which protects striatal learning from decay. A computational version of this theory accounts for a variety of single-cell recording data and some classic behavioral phenomena, includ...

Research paper thumbnail of Decision letter: Motor memories of object dynamics are categorically organized

The ability to predict the dynamics of objects, linking applied force to motion, underlies our ca... more The ability to predict the dynamics of objects, linking applied force to motion, underlies our capacity to perform many of the tasks we carry out on a daily basis. Thus, a fundamental question is how the dynamics of the myriad objects we interact with are organized in memory. Using a custom-built three-dimensional robotic interface that allowed us to simulate objects of varying appearance and weight, we examined how participants learned the weights of sets of objects that they repeatedly lifted. We find strong support for the novel hypothesis that motor memories of object dynamics are organized categorically, in terms of families, based on covariation in their visual and mechanical properties. A striking prediction of this hypothesis, supported by our findings and not predicted by standard associative map models, is that outlier objects with weights that deviate from the family-predicted weight will never be learned despite causing repeated lifting errors. Editor's evaluation This paper provides compelling evidence from several behavioural experiments that recently learned estimates of the mass of novel objects possess a categorical structure in memory. It further links this categorical structure to important aspects of motor control, and provides a compelling window through which to consider the role of multiple systems in the learning and memory of novel object dynamics.

Research paper thumbnail of Declarative strategies persist under increased cognitive load

Psychonomic Bulletin & Review, 2015

When humans simultaneously execute multiple tasks, performance on individual tasks suffers. Compl... more When humans simultaneously execute multiple tasks, performance on individual tasks suffers. Complementing existing theories, this article poses a novel question to investigate interactions between memory systems supporting multi-tasking performance: When a primary and dual task both recruit declarative learning and memory systems, does simultaneous performance of both tasks impair primary task performance because learning in the declarative system is reduced, or because control of the primary task is passed to slower procedural systems? To address this question, participants were trained on either a perceptual categorization task believed to rely on procedural learning or one of three different categorization tasks believed to rely on declarative learning. Task performance was examined with and without a simultaneous dual task thought to recruit working memory and executive attention. To test whether the categories were learned procedurally or declaratively, the response keys were switched after a learning criterion had been reached. Large impairments in performance after switching the response keys are taken to indicate procedural learning, and small impairments are taken to indicate Electronic supplementary material The online version of this article (declarative learning. Our results suggest that the declarative memory categorization tasks (regardless of task difficulty) were learned by declarative systems, regardless of whether they were learned under dual-task conditions.