Novelty detection and repetition suppression in a passive picture viewing task: A possible approach for the evaluation of neuropsychiatric disorders

The applicability of functional magnetic resonance imaging (fMRI) in patients with Alzheimer's disease (AD) or schizophrenia is frequently limited by cognitive impairment, which prevents the adequate execution of complex tasks. An experimental design that puts only minor demands on the patients' cognitive ability but engages disease‐relevant brain structures would be of benefit. Novelty detection and repetition suppression are two basic components of memory that might be used to investigate specific brain areas under these conditions. Novelty detection has been related to hippocampal activation increases. Stimulus repetition related activation decreases (suppression) have been observed in the extrastriate cortex and have been related to perceptual priming. Both processes have been examined primarily in neuroimaging studies with complex cognitive tasks. We used event‐related fMRI to investigate novelty‐ and repetition‐related effects in an attended but passive picture‐viewing task in healthy subjects. The differential activation, detected in the novel vs. repeated contrast, was located in the bilateral anterior hippocampus and in bilateral occipital and inferior‐temporal areas. The hippocampal activation is of interest because medial temporal lobe lesions are key features in AD and schizophrenia. The repetition‐related activation decreases in the extrastriate areas are of potential value in investigating the conflicting results regarding perceptual priming impairment in both disorders. Our results indicate that activation of disease‐relevant brain regions under passive task conditions is possible. This might increase the utility of functional imaging in cognitively impaired patients. Hum. Brain Mapping 17:231–237, 2002. © 2002 Wiley‐Liss, Inc.

[1]  R. McCarley,et al.  A review of MRI findings in schizophrenia , 2001, Schizophrenia Research.

[2]  H. Braak,et al.  Neuropathological stageing of Alzheimer-related changes , 2004, Acta Neuropathologica.

[3]  Alex Martin,et al.  Automatic activation of the medial temporal lobe during encoding: Lateralized influences of meaning and novelty , 1999, Hippocampus.

[4]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[5]  J. Danion,et al.  Explicit memory, repetition priming and cognitive skill learning in schizophrenia , 1994, Schizophrenia Research.

[6]  N. Mulligan,et al.  The role of attention during encoding in implicit and explicit memory. , 1998, Journal of experimental psychology. Learning, memory, and cognition.

[7]  J. Gabrieli,et al.  Word-stem completion priming in healthy aging and Alzheimer's disease: the effects of age, cognitive status, and encoding. , 1999, Neuropsychology.

[8]  G. Glover,et al.  Analysis of a distributed neural system involved in spatial information, novelty, and memory processing , 2000, Human brain mapping.

[9]  G. Orban,et al.  How task-related are the responses of inferior temporal neurons? , 1995, Visual Neuroscience.

[10]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[11]  A. Baddeley,et al.  Memory in schizophrenia: What is impaired and what is preserved? , 1993, Neuropsychologia.

[12]  Daniel L. Schacter,et al.  Priming within and across Modalities: Exploring the Nature of rCBF Increases and Decreases , 2001, NeuroImage.

[13]  E. Tulving,et al.  Novelty encoding networks in the human brain: positron emission tomography data. , 1994, Neuroreport.

[14]  M. Verfaellie,et al.  Preserved priming in auditory perceptual identification in Alzheimer's disease , 2000, Neuropsychologia.

[15]  B. Postle,et al.  Intact implicit memory for novel patterns in Alzheimer's disease. , 1996, Learning & memory (Cold Spring Harbor, N.Y.).

[16]  B Rockstroh,et al.  Increased semantic and repetition priming in schizophrenic patients. , 2001, Journal of abnormal psychology.

[17]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

[18]  Cognitive inhibition and schizophrenic symptom subgroups. , 1996, Schizophrenia bulletin.

[19]  R. Dolan,et al.  Dissociating prefrontal and hippocampal function in episodic memory encoding , 1997, Nature.

[20]  D. Schacter,et al.  Perceptual specificity in visual object priming: functional magnetic resonance imaging evidence for a laterality difference in fusiform cortex , 2001, Neuropsychologia.

[21]  R. Badgaiyan,et al.  Neuroanatomical organization of perceptual memory: An fMRI study of picture priming , 2000, Human brain mapping.

[22]  J. Burke,et al.  Priming deficits in patients with dementia of the Alzheimer type , 1994, Psychological Medicine.

[23]  Lars Nyberg,et al.  Functional Changes in Brain Activity During Priming in Alzheimer's Disease , 2000, Journal of Cognitive Neuroscience.

[24]  Ravi S. Menon,et al.  The effects of visual object priming on brain activation before and after recognition , 2000, Current Biology.

[25]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[26]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[27]  D. Braff,et al.  Schizophrenia patients demonstrate a dissociation on declarative and non-declarative memory tests , 2000, Schizophrenia Research.

[28]  D. Salmon,et al.  Repetition priming with nonverbal stimuli in patients with dementia of the Alzheimer type. , 1998, Neuropsychology.

[29]  Leslie G. Ungerleider,et al.  Complementary neural mechanisms for tracking items in human working memory. , 2000, Science.

[30]  W H Theodore,et al.  Functional mapping of human memory using PET: comparisons of conceptual and perceptual tasks. , 1996, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[31]  F. Miezin,et al.  Functional anatomical studies of explicit and implicit memory retrieval tasks , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Karl J. Friston,et al.  Pharmacological Modulation of Behavioral and Neuronal Correlates of Repetition Priming , 2001, The Journal of Neuroscience.

[33]  Karl J. Friston,et al.  Segregating the functions of human hippocampus. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  K Lehnertz,et al.  Verbal novelty detection within the human hippocampus proper. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  R. Habib.  On the relation between conceptual priming, neural priming, and novelty assessment. , 2001, Scandinavian journal of psychology.

[36]  N. Alpert,et al.  Conscious recollection and the human hippocampal formation: evidence from positron emission tomography. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

[38]  A. Parkin.  Human memory: Novelty, association and the brain , 1997, Current Biology.

[39]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[40]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[41]  Paul J. Harrison.  The neuropathology of schizophrenia , 2008 .

[42]  N. Mulligan,et al.  Attention and perceptual priming in the perceptual identification task. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[43]  R. Knight.  Contribution of human hippocampal region to novelty detection , 1996, Nature.

[44]  Ravi S. Menon,et al.  Repetition priming and the time course of object recognition: an fMRI study. , 1999, Neuroreport.

[45]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[46]  N. Alpert,et al.  Auditory Priming within and across Modalities: Evidence from Positron Emission Tomography , 1999, Journal of Cognitive Neuroscience.