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VOLUME 9, NUMBER 1, FEBRUARY 2000

The Neuropsychological Bases of Category Learning

F. Gregory Ashby1 and Elliott M. Waldron
Department of Psychology, University of California at Santa Barbara, Santa Barbara, California

STRUCTURES Recent evidence sheds light on which neural structures do or do not participate in category learning. Frontal Cortex

Abstract There is a long history of research into how people learn new categories of objects or events. Recent advances have led to new insights about the neuropsychological basis of this critically important cognitive process. In particular, there is now good evidence that the frontal cortex and basal ganglia contribute to category learning, that medial temporal lobe structures make a more minor contribution, and that categorization rules are not represented in visual cortex. There is also strong evidence that normal category learning is mediated by at least two separate systems. A recent neuropsychological theory of category learning that is consistent with these data is described. Keywords categorization; prefrontal cortex; basal ganglia; implicit learning Categorization is the act of assigning objects or events to catego-

ries. It is performed countless times every day, and is among the most important and basic of all decisions. Unfortunately, it is also a fragile process, in the sense that a number of normal and pathological conditions have been shown to cause category-learning deficits. These include normal aging, major depression, Parkinsons disease, Alzheimers disease, Huntingtons disease, strokes, and schizophrenia. Category learning has been long studied, but until recently, little was known about the neural structures and pathways that mediate this fundamental process. Not surprisingly, previous theories of category learning were developed primarily to account for the categorization behavior of healthy university students. However, recent advances in neuroscience and neuropsychology have led to new insights about the neuropsychological bases of category learning. This is an important first step toward the development of a theory that accounts for the categorization behavior not only of healthy young adults, but also of children and older adults, as well as people with various neuropsychological dysfunctions.

The frontal cortex consists roughly of the forward third of the cerebral cortex. With respect to category learning, two especially important structures in this region are the prefrontal cortex and the anterior cingulate, which are thought to be critical for working (i.e., shortterm) memory and executive (i.e., volitional) attentionoperations that one might imagine are important in some types of category learning. So, it is not surprising that there is abundant evidence that the prefrontal cortex is critically important for learning at least some types of category structures. The most well-known such evidence comes from applications of the Wisconsin Card Sorting Test (WCST). This is a widely used neuropsychological test of frontal dysfunction in which participants learn a series of categories that all differ on only a single critical attribute (i.e., symbol color, shape, or number). Patients with lesions of the prefrontal cortex are well known to have deficits on the WCST. This result is so reliable that the WCST is routinely administered to assess for frontal dysfunction. Activation in frontal areas, in-

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cluding the prefrontal cortex and the anterior cingulate, has also been found in the few neuroimaging studies of category learning that have been reported. Visual Cortex Visual cortex refers to all cortical areas associated with visual function. Interest in the hypothesis that category structures are encoded directly in visual cortex has been sparked in recent years by reports of a variety of category-specific agnosias that result from damage to certain high-level visual cortical areas. Category-specific agnosia refers to a reduced ability to recognize exemplars from some specific category, such as inanimate objects (e.g., tools), despite intact ability to categorize most visual stimuli relatively normally. The most widely known of such deficits occur with human faces (i.e., prosopagnosia). Although such category-specific agnosias are consistent with the hypothesis that category structure is represented in visual cortex, they are also generally consistent with the hypothesis that visually similar objects are represented in nearby areas of visual cortex. For example, it is well known that neighboring cells in visual cortex tend to fire to similar stimuli. Thus, damage to some contiguous region of visual cortex is likely to lead to perception deficits within a class of similar stimuli. In fact, specific tests have failed to rule out this similarity hypothesis (e.g., Gaffan & Heywood, 1993). Evidence against the hypothesis that category learning occurs in visual cortex has been obtained in single-cell recording experiments with monkeys. For example, Rolls, Judge, and Sanghera (1977) recorded from cells in a high-level area of the visual (inferotemporal) cortex. In these experiments, one visual stimulus was associated

with reward and one with a mildly aversive taste. After training, the rewards were switched. Thus, in effect, the animals were taught two simple categories (i.e., good and bad), and then the category assignments were switched. If the categories were represented in visual cortex, then the firing properties of visual cortical cells should have changed when the category memberships were switched. However, Rolls et al. found no change in the response of any of these cortical cells, although other similar studies found changes in the responses of cells in other brain areas (e.g., subcortical areas, such as the amygdala). Basal Ganglia The basal ganglia are a collection of subcortical structures that include the caudate nucleus and the putamen (together often called the striatum) and the globus pallidus, among other structures. The case for a basal ganglia contribution to category learning is not as well documented as the case for the prefrontal cortex. Nevertheless, there are some preliminary results. First, there are well-known category-learning deficits in patients with Parkinsons diseasea neurodegenerative disorder that causes extensive dysfunction to the caudate and putamen. Many of these studies used the WCST, but a few recent studies have reported deficits in tasks with more complex category structures (Knowlton, Mangels, & Squire, 1996; Maddox, Filoteo, & Davis, 1999). In Huntingtons disease, there is widespread death of cells in the caudate nucleus, and there are also recent reports of category-learning deficits in patients with Huntingtons disease (Knowlton, Squire, et al., 1996; Maddox et al., 1999). However, such results must be interpreted with caution, because espe-

cially in their later stages, both Parkinsons and Huntingtons disease are also associated with damage to frontal cortical areas. Perhaps the best evidence for a basal ganglia contribution to category learning comes from a long series of lesion studies in rats and monkeys. In primates, virtually all of visual cortex (except area V1) projects (i.e., provides input) directly to the tail of the caudate nucleus, and the cells in this area then project, via the globus pallidus and thalamus, to the prefrontal cortex and more posterior motor areas (e.g., premotor cortex). These projections place the caudate in an ideal position to link percepts and actions, and many researchers have hypothesized that this is its primary role. Many studies have shown that lesions of the tail of the caudate nucleus impair the ability of animals to learn visual discriminations that require one response to one stimulus and a different response to some other stimulus. Because the thalamus and visual cortex are intact in these animals, it is unlikely that their difficulty is in perceiving the stimuli. Rather, it appears that their difficulty is in learning to associate an appropriate response with each stimulus alternative. Technically, such studies are categorization tasks with one exemplar per category. It is difficult to imagine how adding more exemplars to each category could alleviate the deficits caused by caudate lesions, and it is for this reason that the studies of animals with caudate lesions support the hypothesis that the caudate contributes to normal category learning. Medial Temporal Lobe Medial temporal lobe structures, including the hippocampus, the parahippocampal regions, and the entorhinal and pararhinal cortices, are thought to be critical in the con-

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12 solidation of episodic and semantic memories (i.e., memories of episodes and facts, respectively). It might be expected that such memory systems contribute significantly to category learning, especially because a number of current theories assume that people categorize a new stimulus by comparing it to memory representations of previously seen exemplars from each of the possible categories to which it might belong. For this reason, a number of studies have examined how amnesiacs with medial temporal lobe lesions perform in a variety of category-learning tasks. With only a few exceptions, these studies have found normal category learning, even in patients with dense amnesia that resulted from extensive medial temporal lobe lesions (i.e., that included parahippocampal regions, as well as the hippocampus; e.g., Maddox et al., 1999; Squire & Knowlton, 1995). When presented with a stimulus, amnesiacs with medial temporal lobe damage are significantly impaired in judging whether it is old or new (i.e., familiar or unfamiliar), but their ability to assign it to the correct category is essentially normal. Although the issue is far from resolved, these results support the hypothesis that medial temporal lobe structures are not critical for most forms of category learning.

VOLUME 9, NUMBER 1, FEBRUARY 2000

MULTIPLE CATEGORY-LEARNING SYSTEMS The prefrontal cortex and the anterior cingulate project directly to the basal ganglia. Even so, there is reason to believe that, at least in some situations, the two areas contribute to functionally separate category-learning systems. The notion that there may be multiple category-learning systems has a long

history, but recently has been the subject of intense scrutiny. Among those researchers postulating multiple systems, the consensus is that one system learns explicitly and at least one learns implicitly. The explicit system is accessible to consciousness and engages in an explicit reasoning process that may involve hypothesis testing or theory construction and testing. The implicit system is not accessible to conscious awareness. Currently, there is debate as to whether this system uses a procedural- or instance-based memory system. Procedural memory is a phylogenetically ancient system in which simple associations between stimuli and responses are learned, whereas instance-based memories include detailed representations of previously seen category exemplars. Identifying the nature of implicit category learning is an important unsolved problem. There is much evidence consistent with the existence of multiple category-learning systems. For example, there is good evidence of multiple memory systems, and because any category-learning system requires memory, it is feasible that more than one memory system might have its own dedicated category-learning module. More important, a number of studies have found qualitative differences in the way people learn categories that are best separated by an explicit rule (hereafter called explicit tasks) as opposed to how they learn categories that cannot be separated successfully by a salient explicit rule (i.e., implicit tasks). First, learning is often sudden (e.g., insightful) in explicit categorization tasks and gradual (i.e., incremental) in implicit tasks. Second, in the absence of trial-by-trial feedback, people can learn some explicit categorization rules, but there is no evidence that it is possible to learn implicit rules without feedback. Third, there are reports that pa-

tients with frontal lobe damage and people suffering from major depression are impaired in explicit categorization tasks, but not in implicit tasks (Owens et al., 1993; Smith, Tracy, & Murray, 1993). Fourth, a within-subjects comparison found that the ability of healthy elderly people and patients with Parkinsons disease to learn explicit categorization rules was essentially uncorrelated with their ability to learn implicit rules (Ashby, Waldron, Isen, & Noble, 1999).

COVIS In a recent article written with our colleagues, we proposed a theory consistent with these results (Ashby, Alfonso-Reese, Turken, & Waldron, 1998). The theory postulates separate, competing explicit and implicit category-learning systems that are simultaneously active at all times. Depending on the relationship between the categories to be learned, however, one system may dominate the other. We defined explicit rules operationally as those rules that are easy to verbalize, so we called the resulting theory COVIS (COmpetition between Verbal and Implicit Systems). A schematic illustrating the most important neural structures and pathways of COVIS is shown in Figure 1. There are three hierarchical levelscortex, thalamus, and the basal ganglia. The two systems are mediated by parallel loops following the path: cortexcaudateglobus pallidus thalamus. The posterior loop, from visual cortical areas to the tail of the caudate, mediates the implicit system. In humans, all visual cortical areas (except V1) project directly to the tail of the caudate, with about 10,000 visual cortical cells converging on each caudate cell. Cells in the tail of the caudate

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two separate operations (e.g., Owens et al., 1993). First, a new rule (e.g., sort by shape) must be selected from among the alternative salient explicit rules, and second, attention must be switched from the previously active rule to the new rule (e.g., from a rule to sort by color to a rule to sort by shape). COVIS assumes that the selection process is mediated by the anterior cingulate and prefrontal cortex, and that the switching process is mediated within the basal ganglia. Both operations are assumed to be facilitated by dopamine (released from both the substantia nigra and the ventral tegmental area; for more details, see Ashby, Isen, & Turken, 1999).

IMPLICATIONS The results reviewed in this article have a number of important implications. First, the wellreplicated neuropsychological results on category learning are now rich enough that they must be considered when constructing and evaluating new theories about how people learn categories. Second, it is vital to consider carefully the possibility of multiple categorylearning systems when designing new experiments and interpreting their results. In particular, it is important to consider whether the category structures can be discovered via some explicit process, or whether they can only be learned nonexplicitly (i.e., implicitly). Because the properties of the explicit and implicit category-learning systems appear to be different, a failure to consider which system will dominate learning could greatly obfuscate experimental results. There are many important questions left to answer. First, are there more than two category-learning systems? In addition to the explicit and procedural-learning systems

Fig. 1. Schematic illustrating the COVIS model of category learning. Dashed lines indicate dopamine projections. The nucleus accumbens (NAC) is a structure in the ventral striatum that is on a pathway between the ventral tegmental area (VTA) and the substantia nigra (SN). See the text for more details. IT = inferotemporal cortex.

then project to prefrontal or premotor cortex2 (via the globus pallidus and the thalamus). COVIS assumes that each caudate unit functions to associate a category label, or perhaps an abstract motor response, with a large group of visual cortical cells, and that this (procedural) learning process is facilitated by a reward signal mediated by the neurotransmitter dopamine, which is released from the substantia nigra (another structure in the basal ganglia). The explicit system is mediated by an anterior loop, from anterior cingulate and prefrontal cortex to the head of the caudate nucleus,

and then back to the prefrontal cortex. Figure 2 illustrates how this system, which is based on popular models of working memory and executive attention, might operate for a task like the WCST. In Figure 2, the active rule is to sort the cards by the color of the symbols pictured. This rule is maintained in working memory via the bold reverberating loop shown in the figure. If feedback indicates that this rule is incorrect, then the system must implement a different rule, perhaps one that says to sort the cards by the shape of the symbols pictured. There is evidence that implementing a new rule requires

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VOLUME 9, NUMBER 1, FEBRUARY 2000

Notes
1. Address correspondence to F. Gregory Ashby, Department of Psychology, University of California, Santa Barbara, CA 93106; e-mail: ashby@psych.ucsb.edu. 2. For simplicity, Figure 1 shows only direct projections to the prefrontal cortex. 3. The perceptual-priming system (also called the perceptual representation system) is an implicit memory system thought to be localized in sensory (e.g., visual) cortex. Performance with a stimulus is enhanced in this system through simple prior exposure.

References
Ashby, F.G., Alfonso-Reese, L.A., Turken, A.U., & Waldron, E.M. (1998). A neuropsychological theory of multiple systems in category learning. Psychological Review, 105, 442481. Ashby, F.G., Isen, A.M., & Turken, A.U. (1999). A neuropsychological theory of positive affect and its influence on cognition. Psychological Review, 106, 529550. Ashby, F.G., Waldron, E.M., Isen, A.M., & Noble, S. (1999, April). The effects of endogenous dopamine on category learning. Paper presented at the annual meeting of the Cognitive Neuroscience Society, Washington, DC. Gaffan, D., & Heywood, C.A. (1993). A spurious category-specific visual agnosia for living things in normal human and nonhuman primates. Journal of Cognitive Neuroscience, 5, 118 128. Knowlton, B.J., Mangels, J.A., & Squire, L.R. (1996). A neostriatal habit learning system in humans. Science, 273, 13991402. Knowlton, B.J., Squire, L.R., Paulsen, J.S., Swerdlow, N.R., Swenson, M., & Butters, N. (1996). Dissociations within nondeclarative memory in Huntingtons disease. Neuropsychology, 10, 538548. Maddox, W.T., Filoteo, J.V., & Davis, J. (1999, April). Modeling linearly- and nonlinearlyseparable category learning in patients with amnesia, Huntingtons disease, or Parkinsons disease: The role of the hippocampus and basal ganglia. Paper presented at the annual meeting of the Cognitive Neuroscience Society, Washington, DC. Owens, A.M., Roberts, C.R., Hodges, J.R., Summers, B.A., Polkey, C.E., & Robbins, T.W. (1993). Contrasting mechanisms of impaired attentional set shifting in patients with frontal lobe damage or Parkinsons disease. Brain, 116, 11591175. Rolls, E.T., Judge, S.J., & Sanghera, M.K. (1977). Activity of neurones in the inferotemporal cortex of the alert monkey. Brain Research, 130, 229238. Smith, J.D., Tracy, J.I., & Murray, M.J. (1993). Depression and category learning. Journal of Experimental Psychology: General, 122, 331346. Squire, L.R., & Knowlton, B.J. (1995). Learning about categories in the absence of memory. Proceedings of the National Academy of Sciences, USA, 92, 1247012474.

Fig. 2. Schematic illustrating how the explicit system in the COVIS model of category learning operates during the Wisconsin Card Sorting Test. Dashed lines indicate dopamine projections. SN = substantia nigra, VTA = ventral tegmental area.

discussed here, some evidence also points to an instance-based system and perhaps also a perceptualpriming-based system.3 Second, how is learning among the alternative systems coordinated? Third, what is the exact nature of processing within each system? Finally, we caution that the results reviewed in this article pertain only to category learning. There is good reason to believe that categorization behavior that is highly overlearned (i.e., extensively practiced) may have different neuropsychological bases. For example, Parkinsons disease patients are impaired when learning many new categories, but they do not lose their ability to categorize exemplars from highly familiar cat-

egories (e.g., they do not lose categories such as dogs and cats). Recommended Reading
Ashby, F.G., Alfonso-Reese, L.A., Turken, A.U., & Waldron, E.M. (1998). (See References) Ashby, F.G., & Waldron, E.M. (1999). On the nature of implicit categorization. Psychonomic Bulletin & Review, 6, 363378. Knowlton, B.J., Mangels, J.A., & Squire, L.R. (1996). (See References) Owens, A.M., Roberts, C.R., Hodges, J.R., Summers, B.A., Polkey, C.E., & Robbins, T.W. (1993). (See References)
AcknowledgmentsPreparation of this article was supported by Grant SBR9514427 from the National Science Foundation.

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