Pii: s1364-6613(00)01682-x

TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 Graded representations in behavioral
dissociations
Yuko Munakata
Why do people sometimes seem to know things when they are tested in one
a weak representation, but fail another task way, while seeming unaware of this information when tested in a different
designed to measure the same knowledge because it way? Such task-dependent behaviors, or dissociations, often occur in infants
requires a stronger representation. At a conceptual and children, and in adults following brain damage. To explain these
level, representations can be graded in terms of how dissociations, researchers have posited separable knowledge systems that are
‘clean’ they are for signaling the appropriate differentially tapped by various tasks, develop at different rates and can be
information, as opposed to being corrupted by noise selectively impaired. There is an alternative account in which knowledge is
or damage. At the neural level, representations can viewed as graded in nature. Certain tasks tap weaker representations, while
be graded in terms of the number of relevant other tasks require stronger representations, leading to dissociations in
neurons firing, their firing rates and the coherence behavior. The graded representations approach addresses dissociations
observed in perception, attention, memory, executive functioning and
representations depends upon various factors, such language, and has implications for the organization, development and
as the amount of environmental support for them, impairment of our cognitive systems.
the state of development of an individual and theextent of neurological insult.
Knowledge can be highly task dependent. We can On the one hand, the graded representations simultaneously fail one test of knowledge while alternative might seem obvious and not particularly passing another test with flying colors. For example, worthy of review. After all, researchers have long people (with and without brain damage) can fail been aware of the role that task difficulty might play tests of memory for faces by being unable to in dissociations; graded representations could be viewed simply as the mechanism that underlies the nonetheless relearning the correct pairings of effects of difficulty, with stronger representations names and faces more quickly than incorrect needed for more difficult tasks. And, researchers pairings1,2. Adults with prefrontal damage and have thought carefully about how even double children might mistakenly follow old rules for how to dissociations (e.g. one group succeeding on task A behave rather than new rules, while nonetheless but not task B; a second group succeeding on task B demonstrating verbally that they have learned the but not task A) need not imply the existence of new rules3,4. And, people with dyslexia might seem separable underlying systems6–9. Thus, the to know more or less about words depending on the separable systems approach might seem like a straw opponent. On the other hand, prevalent approaches to dissociations across a range of behaviors, or dissociations, might be crucial to domains adopt the notion of separable systems and answering fundamental questions about the ignore the potential role of graded representations.
organization, development and impairment of our Therefore, the graded representations approach cognitive systems. This article explores these issues warrants review. Furthermore, by providing a in the context of dissociations observed in mechanistic basis for behavioral dissociations, the graded representations approach can inform thinking about cognitive systems beyond simply In each domain, the prevalent approach explains caching out notions of task difficulty.
dissociations in terms of separable knowledgesystems that develop at different rates, can be Graded representations in perception
selectively impaired, and contribute differentially to Individuals with optic aphasia have difficulty various tasks. A person might pass one task using naming objects that are presented visually, despite one functioning system, but fail another task being able to gesture the use of visually presented designed to measure the same knowledge because objects and name objects presented auditorally. Most the separate system it taps is underdeveloped or accounts of these dissociations (reviewed in Ref. 10) Yuko Munakata
impaired. An alternative approach explains assume that optic aphasia cannot result from dissociations in terms of knowledge representations damage to a basic system that converts visual that are graded, rather than simply being present or absent, with certain tasks requiring stronger representations, and then semantic representations representations. A person might pass one task using into representations for naming (Fig. 1). Based on http://tics.trends.com 1364-6613/01/$ – see front matter 2001 Elsevier Science Ltd. All rights reserved. PII: S1364-6613(00)01682-X TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 propagated through the system, having a relatively large effect on performance, whereas the auditorynaming task involves weak representations only at the end stage of processing (semantics–naming),resulting in relatively less impairment. Thisprediction is supported by several studies (reviewedin Ref. 10). The model also suggested a method forimproving the performance of individuals by preventing them from responding to a visual objectimmediately. Such a delay improved theperformance of the model dramatically, becauseweak representations from the visual–semanticspathway were strengthened before the semantics–naming pathway operated on them. This prediction has also been supported11.
Fig. 1. Theories of dissociations observed in optic aphasia. According to prevalent accounts (a), the
Graded representations in attention
failure of individuals to name visually presented objects could not arise simply from damage to a Individuals with damage to parietal cortex tend to basic system (indicated by straight arrows). Damage to the visual–semantics pathway is inconsistent neglect the contralateral side of space, instead with the ability of individuals to gesture the use of visually presented objects (which presumably occurs via the visual–semantic–gesture pathway); damage to the semantics–naming pathway is focusing attention on the ipsilateral side12. However, inconsistent with the ability of individuals to name objects presented auditorally (which presumably the evaluation of attention again depends crucially on occurs via the auditory–semantics–naming pathway). Thus, additional systems must be posited how it is measured. Although individuals might be (some of which are shown by curved arrows). According to a graded representations account (b), the poor at identifying contralateral stimuli, they are able observed dissociations could arise owing to partial damage to the visual–semantics and semantics–naming pathways in the basic system. The resulting weak representations most affect to make accurate same–different judgments about tasks that tap both damaged pathways, such as naming visually presented objects (which presumably contralateral and ipsilateral stimuli13,14. The occurs via the visual–semantics–naming pathway). Adapted, with permission, from Ref. 10.
prevalent account of this dissociation was that theperception by the individual of the stimuli was preserved, but a separable system for conscious incorporate additional systems (in some cases awareness of perception was selectively impaired.
That is, individuals could attend to and perceive visual–semantic–naming system to explain the contralateral stimuli, but they could not achieve the dissociations observed in optic aphasia.
conscious awareness of the stimuli required for representations account, these dissociations result In contrast, according to a graded representations from partial damage to both pathways in the basic account, the dissociation following parietal damage visual–semantics–naming system10. Specifically, might result because less visual information damage to the visual–semantics pathway could (a weaker representation) is required for a result in weak semantic representations for visually same–different judgment than for identifying a stimulus14. This graded representations account representations might not be strong enough to drive predicted that: (1) neurologically intact participants a damaged semantics–naming pathway, leading to should show the same dissociation with degraded optic aphasics’ difficulty in naming visually stimuli (e.g. when the stimuli on one side of space are presented objects. However, these weak semantic viewed through a diffusing mask); and (2) the representations might be sufficient to drive an dissociation should disappear in individuals with intact semantics–gesture pathway, which allows parietal damage and neurologically intact optic aphasics to gesture the use of visually participants when the amount of visual information presented objects. Similarly, strong semantic required for the two tasks is equated (e.g. with a representations (e.g. via an intact auditory– forced choice procedure for the identification task).
semantics pathway) might be sufficient to drive the Both of these predictions were confirmed14.
damaged semantics–naming pathway, allowing optic aphasics to name auditorally presented demonstrated how graded activity patterns can govern attention, and how damage to such systems instantiates this graded representations account can lead to deficits observed in neglect15,16.
simulated the dissociations in optic aphasia10.
Furthermore, the model predicted that individuals Graded representations in memory
with optic aphasia should have more difficulty Some of the most compelling dissociations in gesturing the use of visually presented objects than memory occur early in development. For example, naming objects presented auditorally. The gesturing infants demonstrate an apparent memory for hidden task leads to weak representations in the first stage objects within the first few months of life in of processing (visual–semantics) that are then violation-of-expectation studies17,18, while TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 Box 1. Dissociations in memory development
Violation-of-expectation studies build on the assumption that In one of the most well-known studies using this methodf, infants look longer at events that they find novel or unnaturala,b.
infants viewed a drawbridge-like stimulus rotating back and When the novelty or unnaturalness of such events arises based forth, and then saw possible and impossible events involving on objects that have been occluded, the longer looking times of the drawbridge and a block that became occluded by the infants at these events are taken as evidence of their memory for drawbridge (Fig. I). Infants as young as 3.5 months looked the hidden objects. Although these methods are not without longer at the impossible event, indicating some apparent controversy (e.g. see special issues covering debates on those memory for the occluded block. The dissociation between the methods in Refs c–e), they have provided important constraints sensitivity of infants in such violation-of-expectation studies and their failure to search for hidden objects is one of the most Such dissociations are observed even within search tasks. For example, infants appear to reach for toys that are hidden by completely darkening a roomg,h months earlier than they will reach for toys that are hidden by visible occluders in the light. From a graded representations approach, a weak memory of an occluded object might be strong enough to guide a reach in the dark, when there is no direct visual information conflicting with the memory of the object. This same memory, however, might not survive the interference from the visual stimulus of an occluder where the object used to bei. This graded representations account predicts that infants might search more for an object that has been hidden behind a visible occluder if the room lights are then turned off (reducing the interference from the occluder on the weak representation of the hidden object) compared with if the room lights are left on. Preliminary results from our laboratory References
a Fantz, R.L. (1964) Visual experience in infants: decreased attention to familiar patterns relative to novel ones. Science 146, 668–670 b Spelke, E.S. (1985) Preferential looking methods as tools for the study of cognition in infancy. In Measurement of Audition and Vision in the First Year of Postnatal Life (Gottlieb, G. and Krasnegor, N., eds),pp. 323–363, Ablex c Special Issue (2000) Infancy Vol. 1 (4) d Special Issue (1999) Dev. Sci. Vol. 2 (2) e Special Issue (1998) Infant Behav. Dev. 21 (2) f Baillargeon, R. (1987) Object permanence in 3.5- and 4.5-month-old infants.
g Goubet, N. and Clifton, R.K. (1998) Object and event representation in 6-and-a-half-month-old infants. Dev. Psychol. 34, 63–76 Fig. I. An experiment using the violation-of-expectation method to test infants’
h Hood, B. and Willatts, P. (1986) Reaching in the dark to an object’s memory for hidden objectsc. After infants viewed a drawbridge-like stimulus remembered position: evidence for object permanence in 5-month-old rotating back and forth (a), a block was placed in the path of the drawbridge. In the ‘possible’ event (b), the drawbridge rotated to the point where it would touch the infants. Br. J. Dev. Psychol. 4, 57–65 block and then rotated back to its starting point. In the ‘impossible’ event (c), the i Munakata, Y. et al. (1997) Rethinking infant knowledge: toward an adaptive drawbridge appeared to rotate through the space occupied by the block before process account of successes and failures in object permanence tasks.
rotating back to its starting point.
nonetheless failing for several more months to infants successfully retrieve visible objects while search for desired objects that are presented and showing little memory for hidden objects, then hidden (see Box 1). A prevalent account of this demonstrating that their failures with hidden dissociation is that the memory of young infants objects cannot be due solely to problem-solving for hidden objects is intact, but separable systems for acting on this memory are underdeveloped According to a graded representations account, (e.g. a problem-solving system for lifting an the abilities of infants to represent hidden objects occluding cover to retrieve a toy underneath)19–21.
become stronger with development; dissociations in Although problem-solving demands are likely to be memory for hidden objects result because weak part of the problem22, they do not fully explain the representations of hidden objects suffice for some dissociation. When problem-solving demands are tasks but not others23. For example, a weak equated for retrieving visible and hidden toys, representation of a hidden object might allow infants TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 to recognize a strange event with that object in the resolving a conflict (e.g. between the new rule of violation-of-expectation paradigm. Such weak color and the previous rule of shape). In contrast, representations might not suffice for reaching for answering a standard verbal question about the new hidden objects, owing to the greater complexity and rule (e.g. ‘Where do red things go in the color game?’) effort of reaching. However, search failures would does not involve any conflict. This graded not simply reflect deficits in the action system for representations account predicted that the reaching; strong representations of objects (e.g. for dissociation between sorting and verbal measures visible objects) might be sufficient to drive the would disappear when the amount of conflict in the reaching system. This graded representations two tasks was equated (e.g. by adding conflict to the account of dissociations in memory development verbal query by asking, ‘Where do red trucks go in parallels the account of dissociations in optic the color game?’). This prediction has been aphasia. In both cases, particularly poor confirmed in children25. Similarly, a weak prefrontal performance arises when tasks tap the interaction representation of a hidden object might allow between two pathways with weak representations infants to gaze correctly at the location where the (the naming of visually presented objects or reaching object is hidden, whereas a stronger representation for hidden objects), with relatively spared is needed to overcome the prepotent response to performance when tasks tap only one pathway with reach back to a previous hiding location. This graded weak representations (gesturing the use of a visually representations account was instantiated in a presented object, naming an auditorally presented neural network model that (like infants) gazed more object, recognizing an impossible event with an frequently than it reached, allowing the gazing occluded object and reaching for a visible object). A system to make better use of weak representations neural network model has demonstrated how graded representations can support the dissociationsobserved in memory development23. The model also Graded representations in language
predicted that infants would search more for People with phonological dyslexia have difficulty familiar toys than novel toys after they were hidden reading non-words (e.g. ‘nust’), despite being able to read regular words (e.g. ‘mint’) and exception words representations), whereas infants typically showed (e.g. ‘pint’), and to repeat non-words after hearing novelty preferences with visible objects. Preliminary them. Again, this dissociation leads to the work supports this prediction (Y. Munakata, assumption that phonological dyslexia cannot result from damage to a general phonological system;otherwise, people with phonological dyslexia would Graded representations in executive functioning
not be able to read words or repeat non-words after Adults with damage to prefrontal cortex, infants and hearing them. One account of these dissociations children show dissociations in executive functioning, appearing to know things but failing to act information from print (orthography) to sound appropriately on the basis of this knowledge. For (phonology): a word-specific system that is preserved example, adults with prefrontal damage and in phonological dyslexia and a grapheme-to- children can verbally report new rules they have phoneme conversion system that is impaired in learned for sorting cards (e.g. to sort according to the color of the objects on the cards), but incorrectly sort the cards according to previously learned rules representations account, the dissociations observed (e.g. based upon the shape of the objects on the in phonological dyslexia result from the weakening of cards)3,4. Similarly, infants can look to a new location general phonological representations, and the effects where they have watched a toy being hidden, but of these weak representations on an interactive incorrectly reach back to an old location where the language system including orthography and toy was previously hidden26–28. Such compelling semantics5,34,35. Specifically, weak phonological dissociations have suggested that action systems representations might suffice for people to respond might be selectively impaired or underdeveloped appropriately given other (non-phonological) while separable knowledge systems are fully support, as is available for reading words (semantic support) and for repeating non-words after hearing them (auditory support). These weak phonological representations account, prefrontal representations representations might not suffice without such other might be weak because of neurological insult or support, as in the case of reading non-words (no state of development; dissociations in executive semantic or auditory support). This graded functioning result because weak prefrontal representations account predicted that people with representations suffice for some tasks but not phonological dyslexia would show decreasing others25,30–32. For example, stronger representations abilities to repeat words and non-words as the might be required to resolve conflict. Sorting a card semantic and auditory support for them decreased.
(e.g. a red truck) according to a new rule requires This prediction has been confirmed5. Furthermore, TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 Box 2. Explaining dissociations in terms of separable systems
Dissociations in recognition memory (between hippocampus make it well suited for this task measures of recollection and familiarity) might be (e.g. with relatively sparse representations that best understood in terms of the operation of two minimize interference). In contrast, representing the separate systems (the hippocampus and cortex).
underlying structure of the environment requires Consider the case of meeting a new person, and slow, interleaved learning using distributed, overlapping representations. For example, recognizing her. Recollection refers to the retrieval abstracting a general schema for meeting people of specific information about her (such as where (e.g. what kinds of conversation are appropriate, how you were when you met her, what her name is, etc.) closely people stand) requires slow learning over in this recognition process. Familiarity refers to the multiple episodes, collapsing across the differences assessment that she is known (‘I know I’ve seen her of meeting individual people. The cortex appears to before!’), without the recollection of specific be well suited for this task, and can also support familiarity based recognition. Thus, a fundamental Recollection, but not familiarity, is associated with computational trade-off in memory suggests the hippocampal activitya. When people recognize words need for two specialized systems that the that they have studied, hippocampal activity hippocampus and cortex appear to satisfy.
increases if they report recollecting the words, but not Finally, recollection and familiarity are associated if they report that they know that they have seen the with distinct event-related potential components, words without recollecting them (i.e. based on with different timing and spatial topographyd. A familiarity). In fact, hippocampal activity is similarly relatively early frontal FN400 component varies with low for such recognized, non-recollected words as for the familiarity of words, whereas a relatively late new (also non-recollected) words. Furthermore, parietal component varies with the recollection of hippocampal damage impairs recollection but not familiarity, even when difficulty across tasks is References
a Eldridge, L.L. et al. (2000) Remembering episodes: a selective role for the hippocampus during retrieval. Nat. supported the notion of distinct roles for the hippocampus and cortex in memoryc. Recollecting b Holdstock, J.S. et al. Memory dissociations following human particular episodes requires rapid learning with hippocampal damage. Hippocampus (in press) non-overlapping representations. For example, c McClelland, J.L. et al. (1995) Why there are complementary recollecting meeting that particular person requires learning systems in the hippocampus and neocortex: insightsfrom the successes and failures of connectionist models of learning from a single episode and keeping that learning and memory. Psychol. Rev. 102, 419–457 memory distinct from memories of meeting other d Curran, T. (2000) Brain potentials of recollection and people. The anatomy and physiology of the familiarity. Mem. Cognit. 28, 923–938 neural network models have demonstrated how an instantiating graded representations have simulated interactive system of phonology, orthography and a range of dissociations and led to numerous semantics can support typical language processing predictions that have been confirmed empirically.
(without specialized systems for regular words, This approach has shown promise to advance non-words and exception words), and how damage to theorizing about how developmental transitions the system can lead to the dissociations observed in occur, and to inform intervention and rehabilitation.
different types of dyslexia16,34,36–38.
These notions surrounding the nature of our cognitive systems might seem intuitive, or even Conclusions
obvious; they have been part of the cognitive Behavioral dissociations cut across the domains of literature for some time41 and have been emphasized perception, attention, memory, executive functioning in both neural network and dynamic systems and language. These dissociations might be most approaches42. However, numerous theories ignore the salient during development and following brain potential role of graded representations, instead damage, but are also observed in typical, adult treating knowledge as all or nothing and attributing populations (see, for example, Refs 2,14,39,40).
dissociations to deficits in separable systems. It can The graded representations approach provides a be difficult within this kind of framework to think unified framework for understanding behavioral about how developmental transitions occur43 or how dissociations. Behaviors are viewed in terms of an to intervene or rehabilitate. How could children go interactive system that is sensitive to the strength of from nothing to all, and how can individuals improve representations, which can vary based on factors if critical separable pathways are simply missing? such as environmental support, state of development Furthermore, theories within this framework can become unwieldy in the number of separate systems TRENDS in Cognitive Sciences Vol.5 No.7 July 2001 Box 3. Explaining associations as well as dissociations
Theories that posit multiple separable pathways to exception words show some systematicity in the explain dissociations in behavior might have more othography-to-phonology mapping (e.g. in ‘pint,’ the difficulty accounting for related associations than pronunciation of the ‘p’, ‘n’ and ‘t’, and even the graded representations approaches. Consider the pronunciation of the ‘i’ as in ‘pie’ and ‘mind’), despite case of reading, specifically reading regular words, not following the most typical rules of pronunciation (as in ‘mint’). Such ‘neighborhoods’ of similar and These tasks might seem like natural candidates discrepant pronunciations influence the reading of for separable specialized systems. Regular words regular words, exception words and non-words in and non-words can be read according to rules about both typical and brain-damaged populationsc–f.
orthography-to-phonology mappings: ‘mint’ is A single system for reading regular and exception pronounced according to the same rules that govern words and non-words can naturally handle the the pronunciation of ‘hint’ and ‘lint,’ and ‘nust’ similarities across these tasks, and (as described in follows the same rules that govern ‘must’ and ‘rust.’ the main text) can account for the dissociations taken In contrast, exceptions such as ‘pint’ violate such to suggest the existence of separable systems. In rules. And, regular and exception words might be contrast, theories that posit distinct systems to ‘looked up’, based on prior experience, whereas explain the dissociations require special adjustments non-words cannot. Further, behavioral patterns to account for the associations observed across during development and following brain damage suggest separate systems specialized for different reading tasks. People with phonological dyslexia References
a Coltheart, M. et al. (1993) Models of reading aloud: dual-route can read words but have difficulty reading non- and parallel-distributed-processing approaches. Psychol. Rev. words, whereas people with surface dyslexia can read non-words but have difficulty reading b Plaut, D.C. et al. (1996) Understanding normal and impaired exception words. Thus, some theories of word word reading: computational principles in quasi-regular reading posit two separate systems: a rule-based domains. Psychol. Rev. 103, 56–115 c Glushko, R.J. (1979) The organization and activation of system for mapping orthography to phonology (for orthographic knowledge in reading aloud. J. Exp. Psychol. reading regular words and non-words, impaired in phonological dyslexia) and a look-up table for d Jared, D. et al. (1990) The basis of consistency effects in word lexical items (for exception and regular words, naming. J. Mem. Lang. 29, 687–715 Acknowledgements
e Shallice, T. et al. (1983) Reading without semantics. Q. J. Exp. f Taraban, R. and McClelland, J.L. (1987) Conspiracy effects in similarities, across the tasks of reading regular word pronunciation. J. Mem. Lang. 26, 608–631 words, exception words, and non-wordsb. Many g Pinker, S. (1991) Rules of language. Science 253, 530–535 that must be posited to explain the array of Finally, two important caveats to behavioral dissociations observed during development, after dissociations should be noted. First, although damage and in the intact mature system.
graded representations provide a powerful tool forunderstanding dissociations across a range ofdomains, in some cases separable systems might Questions for future research
provide the best explanation (see Box 2). This • Are different causes and consequences associated with different article emphasizes the importance of considering instantiations of gradedness (e.g. firing rates of neurons, coherence of the potential role of graded representations, because in numerous other cases this approach • In other dissociations, such as speech versus gesture44, why might one appears to provide the best explanation, despite behavior require stronger representations than another behavior? being ignored by prevalent accounts. Second, • If a common mechanism (the strengthening of representations) although dissociations are compelling and reliable, supports the ability to carry out new behaviors rather than old behaviors behaviors do often group together. That is, across a range of tasks (e.g. reaching to a new hiding location for a toy performance on one measure of knowledge often rather than an old one, sorting cards according to a new rule rather than correlates with performance on a different an old one), what accounts for the discrepancy in the age when children measure designed to tap the same knowledge.
succeed at these different tasks (one year of age for the hiding task26, These associations might fall out more naturally four years of age for the cardsort task4)? from a graded representations approach with • Could weak representations be strengthened by using them for tasks that interactive systems than from a separable systems approach designed to address dissociations (see • What are further implications for drawing parallels across developing, Box 3). Theoretical frameworks must accommodate brain-damaged, and mature neurologically intact populations? both the associations and the dissociations observedin behavior.
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