Prototype-distortion category learning: a two-phase learning process across a distributed network

This paper reviews a body of work conducted in our laboratory that applies functional magnetic resonance imaging (fMRI) to better understand the biological response and change that occurs during prototype-distortion learning. We review results from two experiments (Little, Klein, Shobat, McClure, & Thulborn, 2004; Little & Thulborn, 2005) that provide support for increasing neuronal efficiency by way of a two-stage model that includes an initial period of recruitment of tissue across a distributed network that is followed by a period of increasing specialization with decreasing volume across the same network. Across the two studies, participants learned to classify patterns of random-dot distortions (Posner & Keele, 1968) into categories. At four points across this learning process subjects underwent examination by fMRI using a category-matching task. A large-scale network, altered across the protocol, was identified to include the frontal eye fields, both inferior and superior parietal lobules, and visual cortex. As behavioral performance increased, the volume of activation within these regions first increased and later in the protocol decreased. Based on our review of this work we propose that: (i) category learning is reflected as specialization of the same network initially implicated to complete the novel task, and (ii) this network encompasses regions not previously reported to be affected by prototype-distortion learning.     

Distinct mechanisms in visual category learning

The ways in which visual categories are learned, and in which well-established categories are represented and retrieved, are fundamental issues of cognitive neuroscience. Researchers have typically studied these issues separately, and the transition from the initial phase of category learning to expertise is poorly characterized. The acquisition of novel categories has been shown to depend on the striatum, hippocampus, and prefrontal cortex, whereas visual category expertise has been shown to involve changes in inferior temporal cortex. The goal of the present experiment is to understand the respective roles of these brain regions in the transition from initial learning to expertise when category judgments are being made. Subjects were explicitly trained, over 2 days, to classify realistic faces. Subjects then performed the categorization task during fMRI scanning, as well as a perceptual matching task, in order to characterize how brain regions respond to these faces when not explicitly categorizing them. We found that, during face categorization, face-selective inferotemporal cortex, lateral prefrontal cortex, and dorsal striatum are more responsive to faces near the category boundary, which are most difficult to categorize. In contrast, the hippocampus and left superior frontal sulcus responded most to faces farthest from the category boundary. These dissociable effects suggest that there are several distinct neural mechanisms involved in categorization, and provide a framework for understanding the contribution of each of these brain regions in categorization.     

Neural correlates of learning and working memory in the primate posterior parietal cortex

The posterior parietal cortex has been traditionally associated with coordinate transformations necessary for interaction with the environment and with visual-spatial attention. More recently, involvement of posterior parietal cortex in other cognitive functions such as working memory and task learning has become evident. Neurophysiological experiments in non-human primates and human imaging studies have revealed neural correlates of memory and learning at the single neuron and at the brain network level. During working memory, posterior parietal neurons continue to discharge and to represent stimuli that are no longer present. This activation resembles the responses of prefrontal neurons, although important differences have been identified in terms of the ability to resist stimulation by distracting stimuli, which is more evident in the prefrontal than the posterior parietal cortex. Posterior parietal neurons also become active during tasks that require the organization of information into larger structured elements and their activity is modulated according to learned context-dependent rules. Neural correlates of learning can be observed in the mean discharge rate and spectral power of neuronal spike trains after training to perform new task sets or rules. These findings demonstrate the importance of posterior parietal cortex in brain networks mediating working memory and learning.     

New knowledge derived from learned knowledge: functional-anatomic correlates of stimulus equivalence

Forming new knowledge based on knowledge established through prior learning is a central feature of higher cognition that is captured in research on stimulus equivalence (SE). Numerous SE investigations show that reinforcing behavior under control of distinct sets of arbitrary conditional relations gives rise to stimulus control by new, derived relations. This investigation examined whether frontal-subcortical and frontal-parietal networks known to support reinforced conditional relations also support derived conditional relations. Twelve adult subjects completed matching-to-sample (MTS) training with correct/wrong feedback to establish four trained conditional relations within two distinct, three-member stimulus classes: (1) A1-->B1, B1-->C1 and (2) A2-->B2, B2-->C2. Afterwards, functional neuroimaging was performed when MTS trials were presented involving matching two identical circles (a sensorimotor control condition), trained relations (A-->B, B-->C), and derived relations: symmetry (B-->A, C-->B), transitivity (A-->C), and equivalence (C-->A). Conditional responding to trained and derived relations was similarly correlated with bilateral activation in the targeted networks. Comparing trained to derived relations, however, highlighted greater activation in several prefrontal regions, the caudate, thalamus, and putamen, which may represent the effects of extended training or feedback present during imaging. Each derived relation also evidenced a unique activation pattern. Collectively, the findings extend the role of frontal-subcortical and frontal-parietal networks to derived conditional relations and suggest that regional involvement varies with the type of derived conditional relation.     

The effect of memory load on cortical activity in the spatial working memory circuit

Accumulating evidence from electrophysiology and neuroimaging studies suggests that spatial working memory is subserved by a network of frontal and parietal regions. In the present study, we parametrically varied the memory set size (one to four spatial locations) of a delayed-response task and applied time-resolved fMRI to study the influence of memory load upon the spatial working memory circuit. Our behavioral results showed that performance deteriorates (lower accuracy and longer reaction time) as memory load increases. Memory load influenced cortical activity during the cue, delay, and response phases of the delayed-response task. Although delay-related activity in many regions increased with increasing memory load, it also was significantly reduced in the middle frontal gyrus and frontal eye fields and leveled off in the parietal areas when memory load increased further. Delayrelated activity in the left posterior parietal cortex was also lower during the error trials, in comparison with the correct trials. Our findings indicate that the delay period activity in the spatial working memory circuit is load sensitive and that the attenuation of this signal is the neural manifestation of performance limitation in the face of excessive memory load.     

参照性交流对关系类别间接性学习的促进作用

以大学生为被试,以4特征虚拟外星生物为实验材料,采用类别的间接性学习范式——个人条件和参照条件,及一个无功能条件,通过三个实验任务（功能预测、自由分类和维度选择）,探讨参照性交流范式下关系类别的间接性学习特点。结果发现：类别的间接性学习条件下,自由分类任务中,被试更倾向于选择关系作为类标准;功能预测的关系类别的间接性学习过程中,参照条件下的功能预测成绩显著高于个人条件,这种差异体现在参照惯例形成的学习过程的中后期;关系类别的间接性学习条件下,参照条件下被试的选择性注意水平显著高于个人条件,这种差异主要表现于选择性注意的指向性方面,而不体现于选择性注意的集中性（对无关维度的抑制）方面。     

Functional connectivity during working memory maintenance

Neurophysiological experiments with monkeys have demonstrated that working memory (WM) is associated with persistent neural activity in multiple brain regions, such as the prefrontal cortex (PFC), the parietal cortex, and posterior unimodal association areas. WM maintenance is believed to require the coordination of these brain regions, which do not function in isolation but, rather, interact to maintain visual percepts that are no longer present in the environment. However, single-unit physiology studies and traditional univariate analyses of functional brain imaging data cannot evaluate interactions between distant brain regions, and so evidence of regional integration during WM maintenance is largely indirect. In this study, we utilized a recently developed multivariate analysis method that allows us to explore functional connectivity between brain regions during the distinct stages of a delayed face recognition task. To characterize the neural network mediating the on-line maintenance of faces, the fusiform face area (FFA) was defined as a seed and was then used to generate whole-brain correlation maps. A random effects analysis of the correlation data revealed a network of brain regions exhibiting significant correlations with the FFA seed during the WM delay period. This maintenance network included the dorsolateral and ventrolateral PFC, the premotor cortex, the intraparietal sulcus, the caudate nucleus, the thalamus, the hippocampus, and occipitotemporal regions. These findings support the notion that the coordinated functional interaction between nodes of a widely distributed network underlies the active maintenance of a perceptual representation.     

Elaborative feedback: Engaging reward and task-relevant brain regions promotes learning in pseudoword reading aloud

Although much is known about the cognitive and neural basis of establishing letter-sound mappings in learning word forms, relatively little is known about what makes for the most effective feedback during this process. We sought to determine the neural basis by which elaborative feedback (EF), which contains both reward-related and content-specific information, may be more helpful than feedback containing only one kind of information (simple positive feedback, PF) or the other (content feedback, CF) in learning orthography-phonology (spelling-sound) mappings for novel letter strings. Compared to CF, EF activated the ventromedial prefrontal cortex, implicated in reward processing. Compared to PF, EF activated the posterior middle temporal, superior temporal, and supramarginal gyri—regions implicated in orthography-phonology conversion. In the same comparison, EF also activated the left fusiform gyrus/visual word form area—implicated in orthographic processing. Also EF, but not CF or PF, modulated activity in the caudate nucleus. In a postscan questionnaire, EF and PF were rated as more pleasant than CF, suggesting that modulation of the caudate for EF may be due to the coupling of reward and skill content. These findings suggest the enhanced effectiveness of EF may be due to concurrent activation of reward-related and task-relevant brain regions.     

The primate working memory networks

Working memory has long been associated with the prefrontal cortex, since damage to this brain area can critically impair the ability to maintain and update mnemonic information. Anatomical and physiological evidence suggests, however, that the prefrontal cortex is part of a broader network of interconnected brain areas involved in working memory. These include the parietal and temporal association areas of the cerebral cortex, cingulate and limbic areas, and subcortical structures such as the mediodorsal thalamus and the basal ganglia. Neurophysiological studies in primates confirm the involvement of areas beyond the frontal lobe and illustrate that working memory involves parallel, distributed neuronal networks. In this article, we review the current understanding of the anatomical organization of networks mediating working memory and the neural correlates of memory manifested in each of their nodes. The neural mechanisms of memory maintenance and the integrative role of the prefrontal cortex are also discussed.     

注意和工作记忆对交错呈现优势的影响

以家族相似性图案为材料,让被试在单任务或双任务条件下以集中呈现或交错呈现的方式进行观察（实验1）或反馈（实验2）学习,记录眼动,探究注意对交错呈现优势的影响,以及工作记忆在其中的作用。发现当进行观察学习时,注意影响交错呈现优势,结果支持区别对比理论和注意衰减理论;当进行反馈学习时,注意的影响还有待进一步探究。同时,工作记忆影响交错呈现优势,但工作记忆并非完全通过影响注意从而影响交错呈现优势。     

Compensatory processing during rule-based category learning in older adults

Healthy older adults typically perform worse than younger adults at rule-based category learning, but better than patients with Alzheimer’s or Parkinson’s disease. To further investigate aging’s effect on rule-based category learning, we monitored event-related potentials (ERPs) while younger and neuropsychologically typical older adults performed a visual category-learning task with a rule-based category structure and trial-by-trial feedback. Using these procedures, we previously identified ERPs sensitive to categorization strategy and accuracy in young participants. In addition, previous studies have demonstrated the importance of neural processing in the prefrontal cortex and the medial temporal lobe for this task. In this study, older adults showed lower accuracy and longer response times than younger adults, but there were two distinct subgroups of older adults. One subgroup showed near-chance performance throughout the procedure, never categorizing accurately. The other subgroup reached asymptotic accuracy that was equivalent to that in younger adults, although they categorized more slowly. These two subgroups were further distinguished via ERPs. Consistent with the compensation theory of cognitive aging, older adults who successfully learned showed larger frontal ERPs when compared with younger adults. Recruitment of prefrontal resources may have improved performance while slowing response times. Additionally, correlations of feedback-locked P300 amplitudes with category-learning accuracy differentiated successful younger and older adults. Overall, the results suggest that the ability to adapt one’s behavior in response to feedback during learning varies across older individuals, and that the failure of some to adapt their behavior may reflect inadequate engagement of prefrontal cortex.     

Learning categories by making predictions: An investigation of indirect category learning

Categories are learned in many ways, but studies of category learning have generally focused on classification learning. This focus may limit the understanding of categorization processes. Two experiments were conducted in which participants learned categories of animals by predicting how much food each animal would eat. We refer to this as indirect category learning, because the task andthe feedback were not directly related to category membership, yet category learning was necessary for good performance in the task. In the first experiment, we compared the performance of participants who learned the categories indirectly with the performance of participants who first learned to classify the objects. In the second experiment, we replicated the basic findings and examined attention to different features during the learning task. In both experiments, participants who learned in the prediction-only condition displayed a broader distribution of attention than participants who learned in the classification-and-prediction condition did. Some participants in the prediction-only group learned the family resemblance structure of the categories, even when a perfect criterial attribute was present. In contrast, participants who first learned to classify the objects tended to learn the criterial attribute.     

Developmental dyslexia and widespread activation across the cerebellar hemispheres

Developmental dyslexia is the most common learning disability in school-aged children with an estimated incidence of five to ten percent. The cause and pathophysiological substrate of this developmental disorder is unclear. Recently, a possible involvement of the cerebellum in the pathogenesis of dyslexia has been postulated. In this study, 15 dyslexic children and 7 age-matched control subjects were investigated by means of functional neuroimaging (fMRI) using a noun-verb association paradigm. Comparison of activation patterns between dyslexic and control subjects revealed distinct and significant differences in cerebral and cerebellar activation. Control subjects showed bilaterally well-defined and focal activation patterns in the frontal and parietal lobes and the posterior regions of the cerebellar hemispheres. The dyslexic children, however, presented widespread and diffuse activations on the cerebral and cerebellar level. Cerebral activations were found in frontal, parietal, temporal and occipital regions. Activations in the cerebellum were found predominantly in the cerebellar cortex, including Crus I, Crus II, hemispheric lobule VI, VII and vermal lobules I, II, III, IV and VII. This preliminary study is the first to reveal a significant difference in cerebellar functioning between dyslexic children and controls during a semantic association task. As a result, we propose a new hypothesis regarding the pathophysiological mechanisms of developmental dyslexia. Given the sites of activation in the cerebellum in the dyslexic group, a defect of the intra-cerebellar distribution of activity is suspected, suggesting a disorder of the processing or transfer of information within the cerebellar cortex.     

Age differences in the neural response to negative feedback

Affective processing is one domain that remains relatively intact in healthy aging. Investigations into the neural responses associated with reward anticipation have revealed that older and younger adults recruit the same midbrain reward regions, but other evidence suggests this recruitment may differ depending on the valence (gain, loss) of the incentive cue. The goal of the current study was to examine functional covariance during gain and loss feedback in younger and healthy older adults. A group of 15 older adults (mean age = 68.5) and 16 younger adults (mean age = 25.4) completed a revised Monetary Incentive Delay task (rMID; Knutson, Westdorp, Kaiser, &; Hommer, 2000) while in the fMRI scanner. The rMID is a reaction time task where successful performance, either gaining a reward or avoiding a loss, is defined by hitting a button during the brief presentation of a visual target. Participants receive gain and loss anticipation cues before each trial and feedback after each trial with four possible outcomes: +$5.00, +0.00, -$5.00, and -Affective processing is one domain that remains relatively intact in healthy aging. Investigations into the neural responses associated with reward anticipation have revealed that older and younger adults recruit the same midbrain reward regions, but other evidence suggests this recruitment may differ depending on the valence (gain, loss) of the incentive cue. The goal of the current study was to examine functional covariance during gain and loss feedback in younger and healthy older adults. A group of 15 older adults (mean age = 68.5) and 16 younger adults (mean age = 25.4) completed a revised Monetary Incentive Delay task (rMID; Knutson, Westdorp, Kaiser, & Hommer, 2000) while in the fMRI scanner. The rMID is a reaction time task where successful performance, either gaining a reward or avoiding a loss, is defined by hitting a button during the brief presentation of a visual target. Participants receive gain and loss anticipation cues before each trial and feedback after each trial with four possible outcomes: +$5.00, +0.00, -$5.00, and -$0.00. Using seed-voxel partial least squares analyses, with seed voxels in the caudate and ventromedial prefrontal cortex, whole-brain functional covariance revealed that younger and older adults engage the same network of regions to support general feedback processing. However, older adults engaged two additional networks to support processing of negative feedback, gain_miss (+0), loss_miss (-$5), and loss_hit (?0), specifically. These findings are in line with theories of a positivity effect in aging and may have implications for reward-stimulus learning and decision making following performance-contingent negative feedback.     

Greater Intermanual Transfer in the Elderly Suggests Age-Related Bilateral Motor Cortex Activation Is Compensatory

ABSTRACT. Hemispheric lateralization of movement control diminishes with age; whether this is compensatory or maladaptive is debated. The authors hypothesized that if compensatory, bilateral activation would lead to greater intermanual transfer in older subjects learning tasks that activate the cortex unilaterally in young adults. They studied 10 young and 14 older subjects, learning a unimanual visuomotor task comprising a feedforward phase, where there is unilateral cortical activation in young adults, and a feedback phase, which activates the cortex bilaterally in both age groups. Increased intermanual transfer was demonstrated in older subjects during feedforward learning, with no difference between groups during feedback learning. This finding is consistent with bilateral cortical activation being compensatory to maintain performance despite declining computational efficiency in neural networks.     

Perseverative interference with object-in-place scene learning in rhesus monkeys with bilateral ablation of ventrolateral prefrontal cortex

Surgical disconnection of the frontal cortex and inferotemporal cortex severely impairs many aspects of visual learning and memory, including learning of new object-in-place scene memory problems, a monkey model of episodic memory. As part of a study of specialization within prefrontal cortex in visual learning and memory, we tested monkeys with bilateral ablations of ventrolateral prefrontal cortex in object-in-place scene learning. These monkeys were mildly impaired in scene learning relative to their own preoperative performance, similar in severity to that of monkeys with bilateral ablation of orbital prefrontal cortex. An analysis of response types showed that the monkeys with lesions were specifically impaired in responding to negative feedback during learning: The post-operative increase in errors was limited to trials in which the first response to each new problem, made on the basis of trial and error, was incorrect. This perseverative pattern of deficit was not observed in the same analysis of response types in monkeys with bilateral ablations of the orbital prefrontal cortex, who were equally impaired on trials with correct and incorrect first responses. This may represent a specific signature of ventrolateral prefrontal involvement in episodic learning and memory.     

青老年组不同难度下心算活动的脑功能磁共振成像研究

应用功能磁共振成像技术研究不同心算难度下脑区的活动以及年龄的影响。14名志愿者（20～29岁青年和60～69岁老年被试各7名）参加了该实验。实验任务为2个难度水平的连续减法心算,分别为1000—3和1000—17。结果表明：（1）心算加工激活了额叶和顶叶的许多脑区;（2）大脑左半球是心算加工的优势半球,但随着心算难度加大,大脑一侧化程度下降,而年老加剧了这一趋势;（3）青年组进行简单心算（1000—3）时,额中回未见明显激活,而老年组进行简单心算时,该脑区被明显激活。总体上,额叶和顶叶在心算活动中起着重要作用,而任务难度和年龄对心算加工时脑活动的影响以额中回区最为明显。     

Serial reaction time performance following right parietal lobe damage

The serial reaction time task (SRT) is used to assess implicit sequence learning. Neuroimaging studies implicate parietal involvement; however, the necessity of this area is unclear. We tested six unilateral right parietal patients and compared their performance to matched controls. Both groups showed similar levels of learning and explicit awareness. Two patients with the largest lesions extending into either frontal or cerebellar regions showed no learning. These data suggest that implicit sequence learning can occur despite damage to the right parietal lobe.     

反馈延迟对信息整合类别学习的影响：视觉项目精准性的调节作用

研究旨在探究更精确的视觉项目表征能否消除延迟反馈对信息整合学习的损害。实验采用2（视觉项目表征精确性：精确/非精确）×2（反馈延迟：即时反馈/延迟反馈）组间设计,结果发现无论有无延迟反馈,精确的项目表征条件下类别学习成绩都显著高于非精确条件,精确性与反馈延迟存在交互作用。采用状态痕迹分析进一步证明精确性显著影响信息整合类别学习的稳定性。在反馈延迟条件下,精确的视觉项目表征能提高信息整合类别学习的成绩。     

Neural correlates of visuospatial consciousness in 3D default space: Insights from contralateral neglect syndrome

One of the most compelling questions still unanswered in neuroscience is how consciousness arises. In this article, we examine visual processing, the parietal lobe, and contralateral neglect syndrome as a window into consciousness and how the brain functions as the mind and we introduce a mechanism for the processing of visual information and its role in consciousness. We propose that consciousness arises from integration of information from throughout the body and brain by the thalamus and that the thalamus reimages visual and other sensory information from throughout the cortex in a default three-dimensional space in the mind. We further suggest that the thalamus generates a dynamic default three-dimensional space by integrating processed information from corticothalamic feedback loops, creating an infrastructure that may form the basis of our consciousness. Further experimental evidence is needed to examine and support this hypothesis, the role of the thalamus, and to further elucidate the mechanism of consciousness.