Effect of schizophrenia on frontotemporal activity during word encoding and recognition: a PET cerebral blood flow study.

OBJECTIVE Neuropsychological studies have shown that deficits in verbal episodic memory in schizophrenia occur primarily during encoding and retrieval stages of information processing. The current study used positron emission tomography to examine the effect of schizophrenia on change in cerebral blood flow (CBF) during these memory stages. METHOD CBF was measured in 23 healthy comparison subjects and 23 patients with schizophrenia during four conditions: resting baseline, motor baseline, word encoding, and word recognition. The motor baseline was used as a reference that was subtracted from encoding and recognition conditions by using statistical parametric mapping. RESULTS Patients' performance was similar to that of healthy comparison subjects. During word encoding, patients showed reduced activation of left prefrontal and superior temporal regions. Reduced left prefrontal activation in patients was also seen during word recognition, and additional differences were found in the left anterior cingulate, left mesial temporal lobe, and right thalamus. Although patients' performance was similar to that of healthy comparison subjects, left inferior prefrontal activation was associated with better performance only in the comparison subjects. CONCLUSIONS Left frontotemporal activation during episodic encoding and retrieval, which is associated with better recognition in healthy people, is disrupted in schizophrenia despite relatively intact recognition performance and right prefrontal function. This may reflect impaired strategic use of semantic information to organize encoding and facilitate retrieval.

[1]  J. Overall,et al.  The Brief Psychiatric Rating Scale , 1962 .

[2]  A. Paivio,et al.  Concreteness, imagery, and meaningfulness values for 925 nouns. , 1968, Journal of experimental psychology.

[3]  F. Craik,et al.  Levels of Pro-cessing: A Framework for Memory Research , 1975 .

[4]  W D Obrist,et al.  Sex and handedness differences in cerebral blood flow during rest and cognitive activity. , 1982, Science.

[5]  E. Tulving Elements of episodic memory , 1983 .

[6]  L. McClain Encoding and Retrieval in Schizophrenics' Free Recall , 1983, The Journal of nervous and mental disease.

[7]  A. Calev Recall and recognition in chronic nondemented schizophrenics: use of matched tasks. , 1984, Journal of abnormal psychology.

[8]  D. Weinberger,et al.  Physiologic dysfunction of dorsolateral prefrontal cortex in schizophrenia. I. Regional cerebral blood flow evidence. , 1986, Archives of general psychiatry.

[9]  T. Goldberg,et al.  Further evidence for dementia of the prefrontal type in schizophrenia? A controlled study of teaching the Wisconsin Card Sorting Test. , 1987, Archives of general psychiatry.

[10]  D. Delis,et al.  Sex differences in verbal learning , 1988 .

[11]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[12]  M. Posner,et al.  Localization of cognitive operations in the human brain. , 1988, Science.

[13]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[14]  B. Bogerts The Neuropathology of Schizophrenia , 1990 .

[15]  F. Wood,et al.  Hypofrontal vs. hypo-Sylvian blood flow in schizophrenia. , 1990, Schizophrenia bulletin.

[16]  R. Gur,et al.  Volunteers for biomedical research. Recruitment and screening of normal controls. , 1991, Archives of general psychiatry.

[17]  R. Gur,et al.  Relations among clinical scales in schizophrenia. , 1991, The American journal of psychiatry.

[18]  Joel S. Karp,et al.  Effect of increased axial field of view on the performance of a volume PET scanner , 1991, Conference Record of the 1991 IEEE Nuclear Science Symposium and Medical Imaging Conference.

[19]  T. Goldberg,et al.  Forms of memory failure in schizophrenia. , 1992 .

[20]  R. Gur,et al.  Neurobehavioral probes for physiologic neuroimaging studies. , 1992, Archives of general psychiatry.

[21]  Sohee Park,et al.  Schizophrenics show spatial working memory deficits. , 1992, Archives of general psychiatry.

[22]  ChrisD . Frith The Cognitive Neuropsychology of Schizophrenia , 1992 .

[23]  S. Resnick Matching for education in studies of schizophrenia. , 1992, Archives of general psychiatry.

[24]  N C Andreasen,et al.  Hypofrontality in neuroleptic-naive patients and in patients with chronic schizophrenia. Assessment with xenon 133 single-photon emission computed tomography and the Tower of London. , 1992, Archives of general psychiatry.

[25]  W T Carpenter,et al.  Limbic system abnormalities identified in schizophrenia using positron emission tomography with fluorodeoxyglucose and neocortical alterations with deficit syndrome. , 1992, Archives of general psychiatry.

[26]  S. Potkin,et al.  Cortical-striatal-thalamic circuits and brain glucose metabolic activity in 70 unmedicated male schizophrenic patients. , 1993, American Journal of Psychiatry.

[27]  R. Heinrichs,et al.  Neurocognitive subtypes of chronic schizophrenia , 1993, Schizophrenia Research.

[28]  D. Braff Information processing and attention dysfunctions in schizophrenia. , 1993, Schizophrenia bulletin.

[29]  Joel S. Karp,et al.  The countrate performance of the volume imaging PENN-PET scanner , 1994, IEEE Trans. Medical Imaging.

[30]  R. Gur,et al.  Cerebral blood flow in schizophrenia: Effects of memory processing on regional activation , 1994, Biological Psychiatry.

[31]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

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

[33]  Jane S. Paulsen,et al.  The nature of learning and memory impairments in schizophrenia , 1995, Journal of the International Neuropsychological Society.

[34]  Jemett L. Desmond,et al.  Semantic encoding and retrieval in the left inferior prefrontal cortex: a functional MRI study of task difficulty and process specificity , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  Karl J. Friston,et al.  Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia , 1995, Nature.

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

[38]  C. Huron,et al.  Impairment of recognition memory with, but not without, conscious recollection in schizophrenia. , 1995, The American journal of psychiatry.

[39]  Alan C. Evans,et al.  Functional activation of the human ventrolateral frontal cortex during mnemonic retrieval of verbal information. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[40]  B. Gulyás,et al.  Visual memory, visual imagery, and visual recognition of large field patterns by the human brain: functional anatomy by positron emission tomography. , 1995, Cerebral cortex.

[41]  R. Buckner Beyond HERA: Contributions of specific prefrontal brain areas to long-term memory retrieval , 1996, Psychonomic bulletin & review.

[42]  M S Buchsbaum,et al.  PET and MRI of the thalamus in never-medicated patients with schizophrenia. , 1996, The American journal of psychiatry.

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

[44]  T. Goldberg,et al.  Effects of neuroleptic medications on the cognition of patients with schizophrenia: a review of recent studies. , 1996, The Journal of clinical psychiatry.

[45]  Karl J. Friston,et al.  The Trouble with Cognitive Subtraction , 1996, NeuroImage.

[46]  Randy L. Buckner,et al.  What does neuroimaging tell us about the role of prefrontal cortex in memory retrieval , 1996 .

[47]  C. Carter,et al.  Spatial working memory deficits and their relationship to negative symptoms in unmedicated schizophrenia patients , 1996, Biological Psychiatry.

[48]  S. Houle,et al.  Activation of medial temporal structures during episodic memory retrieval , 1996, Nature.

[49]  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.

[50]  N C Andreasen,et al.  Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  G. Pearlson,et al.  Schizophrenia: A Disease of Heteromodal Association Cortex? , 1996, Neuropsychopharmacology.

[52]  P. Liddle Functional imaging--schizophrenia. , 1996, British medical bulletin.

[53]  M S Buchsbaum,et al.  Decreased anterior cingulate gyrus metabolic rate in schizophrenia. , 1997, The American journal of psychiatry.

[54]  J M Gorman,et al.  Mechanisms underlying memory impairment in schizophrenia , 1997, Psychological Medicine.

[55]  Jonathan S. Lewin,et al.  Functional magnetic resonance imaging in schizophrenia: initial methodology and evaluation of the motor cortex , 1997, Psychiatry Research: Neuroimaging.

[56]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[57]  N. Andreasen,et al.  Hypofrontality in schizophrenia: distributed dysfunctional circuits in neuroleptic-naïve patients , 1997, The Lancet.

[58]  N. Andreasen,et al.  The effect of antipsychotic medication on relative cerebral blood perfusion in schizophrenia: Assessment with technetium-99m hexamethyl-propyleneamine oxime single photon emission computed tomography , 1997, Biological Psychiatry.

[59]  R. Kawashima,et al.  Different roles of the left and right parahippocampal regions in verbal recognition: a PET study , 1997 .

[60]  M. Mintun,et al.  PET brain mapping study of auditory verbal supraspan memory versus visual fixation in schizophrenia , 1997, Biological Psychiatry.

[61]  Sensorimotor cortex lateralization is anomalous in patients with schizophrenia: A whole brain fMRI study , 1997 .

[62]  Alex Martin,et al.  Modulation of human medial temporal lobe activity by form, meaning, and experience , 1997, Hippocampus.

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

[64]  Ruben C. Gur,et al.  Lateralized Changes in Regional Cerebral Blood Flow during Performance of Verbal and Facial Recognition Tasks: Correlations with Performance and “Effort” , 1997, Brain and Cognition.

[65]  Lars Nyberg,et al.  Mapping episodic memory , 1998, Behavioural Brain Research.

[66]  E. Tulving,et al.  Hippocampal PET activations of memory encoding and retrieval: The HIPER model , 1998, Hippocampus.

[67]  P. Goldman-Rakic,et al.  Cortical dysfunction in schizophrenia during auditory word and tone working memory demonstrated by functional magnetic resonance imaging. , 1998, Archives of general psychiatry.

[68]  Karl J. Friston,et al.  Brain activations in schizophrenia during a graded memory task studied with functional neuroimaging. , 1998, Archives of general psychiatry.

[69]  J. Cohen,et al.  Functional hypofrontality and working memory dysfunction in schizophrenia. , 1998, The American journal of psychiatry.

[70]  D. Schacter,et al.  Functional–Anatomic Study of Episodic Retrieval Using fMRI I. Retrieval Effort versus Retrieval Success , 1998, NeuroImage.

[71]  A. Alavi,et al.  Frontotemporal cerebral blood flow change during executive and declarative memory tasks in schizophrenia: a positron emission tomography study. , 1998, Neuropsychology.

[72]  Francis Eustache,et al.  The Functional Neuroanatomy of Episodic Memory: The Role of the Frontal Lobes, the Hippocampal Formation, and Other Areas , 1998, NeuroImage.

[73]  N. Alpert,et al.  Impaired recruitment of the hippocampus during conscious recollection in schizophrenia , 1998, Nature Neuroscience.

[74]  G T Stebbins,et al.  Working and strategic memory deficits in schizophrenia. , 1998, Neuropsychology.

[75]  Karl J. Friston,et al.  A multimodal language region in the ventral visual pathway , 1998, Nature.

[76]  R. Coppola,et al.  Functional Magnetic Resonance Imaging Brain Mapping in Psychiatry: Methodological Issues Illustrated in a Study of Working Memory in Schizophrenia , 1998, Neuropsychopharmacology.

[77]  T. Robbins,et al.  Impaired generation and use of strategy in schizophrenia: evidence from visuospatial and verbal tasks , 1998, Psychological Medicine.

[78]  S. Paradiso,et al.  Recalling word lists reveals "cognitive dysmetria" in schizophrenia: a positron emission tomography study. , 1999, The American journal of psychiatry.

[79]  N. Alpert,et al.  Functional imaging of memory retrieval in deficit vs nondeficit schizophrenia. , 1999, Archives of general psychiatry.

[80]  D. Schacter,et al.  Medial temporal lobe activations in fMRI and PET studies of episodic encoding and retrieval , 1999, Hippocampus.

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

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

[83]  M. Botvinick,et al.  The Contribution of the Anterior Cingulate Cortex to Executive Processes in Cognition , 1999, Reviews in the neurosciences.

[84]  J. Danion,et al.  Functional mechanisms underlying impaired recognition memory and conscious awareness in patients with schizophrenia. , 1999, Archives of general psychiatry.

[85]  S. Marder,et al.  Risperidone versus haloperidol on secondary memory: can newer medications aid learning? , 1999, Schizophrenia bulletin.

[86]  Karl J. Friston,et al.  Abnormal neural integration related to cognition in schizophrenia , 1999, Acta psychiatrica Scandinavica. Supplementum.

[87]  Philip K. McGuire,et al.  Attenuated frontal activation in schizophrenia may be task dependent 1 This paper was given at the 9th Biennial Winter Workshop on Schizophrenia, February 1998, Davos, Switzerland. 1 , 1999, Schizophrenia Research.

[88]  O. Saitoh,et al.  Neural correlates of memory organization deficits in schizophrenia A single photon emission computed tomography study with 99mTc-ethyl-cysteinate dimer during a verbal learning task , 2000, Schizophrenia Research.

[89]  Ruben C. Gur,et al.  Hemispheric Activation of Anterior and Inferior Prefrontal Cortex during Verbal Encoding and Recognition: A PET Study of Healthy Volunteers , 2000, NeuroImage.

[90]  C Ranganath,et al.  Neural correlates of memory retrieval and evaluation. , 2000, Brain research. Cognitive brain research.

[91]  Igor Nenadic,et al.  Hypofrontality in unmedicated schizophrenia patients studied with PET during performance of a serial verbal learning task , 2000, Schizophrenia Research.