Human Brain Regions Involved in Visual Categorization

Categorization of dot patterns is a frequently used paradigm in the behavioral study of natural categorization. To determine the human brain regions involved in categorization, we used Positron Emission Tomography to compare regional Cerebral Blood Flow patterns in two tasks employing patterns that consisted of nine dots. In the categorization task, subjects categorized novel exemplars of two categories, generated by distorting two prototypes, and other random dot patterns. In the control task, subjects judged the position of similarly distorted patterns. Each task was presented at two matched levels of difficulty. Fixation of the fixation target served as baseline condition. The categorization task differentially activated the orbitofrontal cortex and two dorsolateral prefrontal regions. These three prefrontal regions were equally weakly active in the position discrimination task and the baseline condition. The intraparietal sulcus was activated in both tasks, albeit significantly less in the position discrimination than in the categorization task. A similar activation pattern was present in the neostriatum. Task difficulty had no effect. These functional imaging results show that the dot-pattern categorization task strongly engages prefrontal and parietal cortical areas. The activation of prefrontal cortex during visual categorization in humans agrees with the recent finding of category-related responses in macaque prefrontal neurons.

[1]  S. Wise,et al.  Role of the Hippocampal System in Conditional Motor Learning: Mapping Antecedents to Action , 1999, Hippocampus.

[2]  R. Elliott,et al.  Activation of Different Anterior Cingulate Foci in Association with Hypothesis Testing and Response Selection , 1998, NeuroImage.

[3]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[4]  E. Stein,et al.  A parametric manipulation of central executive functioning. , 2000, Cerebral cortex.

[5]  W. Schultz,et al.  Modifications of reward expectation-related neuronal activity during learning in primate orbitofrontal cortex. , 2000, Journal of neurophysiology.

[6]  T. Shallice,et al.  Deficits in strategy application following frontal lobe damage in man. , 1991, Brain : a journal of neurology.

[7]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[9]  Shawn W. Ell,et al.  The neurobiology of human category learning , 2001, Trends in Cognitive Sciences.

[10]  R. Elliott,et al.  Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals , 1999, The Journal of Neuroscience.

[11]  Guy Marchal,et al.  Multimodality image registration by maximization of mutual information , 1997, IEEE Transactions on Medical Imaging.

[12]  R. Passingham,et al.  The prefrontal cortex: response selection or maintenance within working memory? , 2000, 5th IEEE EMBS International Summer School on Biomedical Imaging, 2002..

[13]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[14]  M. Mishkin,et al.  Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys , 1997, Neuropsychologia.

[15]  Y. Miyashita,et al.  No‐go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging , 1998, The European journal of neuroscience.

[16]  Y. Miyashita,et al.  Contribution of working memory to transient activation in human inferior prefrontal cortex during performance of the Wisconsin Card Sorting Test. , 1999, Cerebral cortex.

[17]  A. Damasio,et al.  Insensitivity to future consequences following damage to human prefrontal cortex , 1994, Cognition.

[18]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  G Brix,et al.  Performance evaluation of a whole-body PET scanner using the NEMA protocol. National Electrical Manufacturers Association. , 1997, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[20]  G. Orban,et al.  Separate neural correlates for the mnemonic components of successive discrimination and working memory tasks. , 2001, Cerebral cortex.

[21]  E. Rolls The orbitofrontal cortex and reward. , 2000, Cerebral cortex.

[22]  Ivan Toni,et al.  Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study , 1999, Experimental Brain Research.

[23]  M. Posner,et al.  On the genesis of abstract ideas. , 1968, Journal of experimental psychology.

[24]  P. Goldman-Rakic,et al.  Human Brain Mapping 6:14–32(1998) � Dissociation of Mnemonic and Perceptual Processes During Spatial and Nonspatial Working Memory Using fMRI , 2022 .

[25]  N. Kanwisher,et al.  The Generality of Parietal Involvement in Visual Attention , 1999, Neuron.

[26]  Edward E. Smith,et al.  Categories and concepts , 1984 .

[27]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[28]  H. Damasio,et al.  Dissociation Of Working Memory from Decision Making within the Human Prefrontal Cortex , 1998, The Journal of Neuroscience.

[29]  J. Allman,et al.  Mapping human visual cortex with positron emission tomography , 1986, Nature.

[30]  T. Robbins,et al.  Choosing between Small, Likely Rewards and Large, Unlikely Rewards Activates Inferior and Orbital Prefrontal Cortex , 1999, The Journal of Neuroscience.

[31]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[32]  Karl J. Friston,et al.  Assessing the significance of focal activations using their spatial extent , 1994, Human brain mapping.

[33]  A. Damasio,et al.  Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. , 1996, Cerebral cortex.

[34]  J. Mugler,et al.  Three‐dimensional magnetization‐prepared rapid gradient‐echo imaging (3D MP RAGE) , 1990, Magnetic resonance in medicine.

[35]  P. Reber,et al.  Contrasting cortical activity associated with category memory and recognition memory. , 1998, Learning & memory.

[36]  Paul Kinahan,et al.  Analytic 3D image reconstruction using all detected events , 1989 .

[37]  R. Passingham,et al.  Learning Arbitrary Visuomotor Associations: Temporal Dynamic of Brain Activity , 2001, NeuroImage.

[38]  Bruce R. Rosen,et al.  Activity in Ventrolateral and Mid-Dorsolateral Prefrontal Cortex during Nonspatial Visual Working Memory Processing: Evidence from Functional Magnetic Resonance Imaging , 2000, NeuroImage.

[39]  L. Squire,et al.  The learning of categories: parallel brain systems for item memory and category knowledge. , 1993, Science.

[40]  R. Vogels Categorization of complex visual images by rhesus monkeys. Part 2: single‐cell study , 1999, The European journal of neuroscience.

[41]  Hidenao Fukuyama,et al.  Cerebral activation during performance of a card sorting test , 1996 .

[42]  Russell A Poldrack,et al.  Hemispheric asymmetries and individual differences in visual concept learning as measured by functional MRI , 2000, Neuropsychologia.

[43]  M. Mishkin,et al.  Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity , 1970, Experimental Brain Research.

[44]  A. Benton,et al.  Frontal Lobe Function and Dysfunction , 1991 .

[45]  G A Orban,et al.  Regional brain activity during shape recognition impaired by a scopolamine challenge to encoding , 1999, The European journal of neuroscience.

[46]  T. Bussey,et al.  Role of prefrontal cortex in a network for arbitrary visuomotor mapping , 2000, Experimental Brain Research.

[47]  A. Damasio,et al.  Emotion, decision making and the orbitofrontal cortex. , 2000, Cerebral cortex.

[48]  Gregory Ashby,et al.  A neuropsychological theory of multiple systems in category learning. , 1998, Psychological review.

[49]  C. Carter,et al.  Complementary Category Learning Systems Identified Using Event-Related Functional MRI , 2000, Journal of Cognitive Neuroscience.

[50]  N. J. Herrod,et al.  Redefining the functional organization of working memory processes within human lateral prefrontal cortex , 1999, The European journal of neuroscience.

[51]  M. Petrides Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man , 1985, Neuropsychologia.

[52]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[53]  F. Rieke,et al.  An AC bridge readout for bolometric detectors , 1988 .

[54]  L. Komatsu Recent views of conceptual structure , 1992 .

[55]  M. Posner,et al.  Perceived distance and the classification of distorted patterns. , 1967, Journal of experimental psychology.

[56]  D. Homa Prototype abstraction and classification of new instances as a function of number of instances defining the prototype , 1973 .

[57]  P J Reber,et al.  Cortical areas supporting category learning identified using functional MRI. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Gregory Ashby,et al.  Suboptimality in human categorization and identification. , 2001, Journal of experimental psychology. General.

[59]  Probing the brain with DNA chips , 1999, Nature Neuroscience.

[60]  M. Corbetta,et al.  Areas Involved in Encoding and Applying Directional Expectations to Moving Objects , 1999, The Journal of Neuroscience.

[61]  D. Homa,et al.  Category Breadth and the Abstraction of Prototypical Information. , 1976 .

[62]  J. Hollerman,et al.  Reward processing in primate orbitofrontal cortex and basal ganglia. , 2000, Cerebral cortex.

[63]  R. Passingham,et al.  Specialisation within the prefrontal cortex: the ventral prefrontal cortex and associative learning , 2000, Experimental Brain Research.

[64]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[65]  E. Rolls,et al.  Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[66]  L. Squire,et al.  Learning about categories in the absence of memory. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[67]  Richard Coppola,et al.  Physiological activation of a cortical network during performance of the Wisconsin Card Sorting Test: A positron emission tomography study , 1995, Neuropsychologia.

[68]  A. Owen The Functional Organization of Working Memory Processes Within Human Lateral Frontal Cortex: The Contribution of Functional Neuroimaging , 1997, The European journal of neuroscience.

[69]  R. Elliott,et al.  Ventromedial prefrontal cortex mediates guessing , 1999, Neuropsychologia.