Subcortical Loop Activation during Selection of Currently Relevant Memories

Clinical studies on spontaneous confabulation and imaging studies with healthy subjects indicate that the anterior limbic system, in particular, the orbitofrontal cortex (OFC), is necessary to adjust thought and behavior to current reality. It appears to achieve this by continuously suppressing activated memories that do not pertain to ongoing reality, even before their content is consciously recognized. In the present study, we explored through what anatomical connections the OFC exerts this influence. Healthy subjects were scanned with H2 15O PET as they performed four blocks of continuous recognition tasks, each block composed of a different type of stimuli (meaningful designs, geometric designs, words, nonwords). Within each block, three runs composed of exactly the same picture series, arranged in different order each time, were made. Subjects were asked to indicate item recurrences only within the currently ongoing run and to disregard familiarity from previous runs. In the combined first runs, in which all items were initially new and responses could be based on familiarity judgement (with repeated items) alone, we found medial temporal and right orbitofrontal activation. In the combined third runs, when all items were already known and selection of currently relevant memories was required, we found left orbitofrontal activation contingent with distinct activation of the ventral striatum, head and body of the caudate nucleus, substantia nigra, and medial thalamus. The study indicates that the OFC influences the cortical representation of memories through subcortical connections including the basal ganglia and the thalamus. The data are compatible with a role of the dopaminergic reward system in the monitoring of ongoing reality in thinking.

[1]  Karl J. Friston,et al.  Dissociable Neural Responses in Human Reward Systems , 2000, The Journal of Neuroscience.

[2]  A. Schnider,et al.  Dopamine inhibition and the adaptation of behavior to ongoing reality , 2004, Neuroreport.

[3]  E. Lynd-Balta,et al.  The orbital and medial prefrontal circuit through the primate basal ganglia , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  A. Schnider,et al.  The mechanisms of spontaneous and provoked confabulations. , 1996, Brain : a journal of neurology.

[5]  C W Hess,et al.  Memory without context: amnesia with confabulations after infarction of the right capsular genu. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[6]  G. Percheron,et al.  [Informational neuro-morphology of the cortico-ponto-cerebello-thalamo-cortical system in primates (compared with basal ganglia system)]. , 1993, Revue neurologique.

[7]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[8]  A. Schnider,et al.  Disorientation in amnesia. A confusion of memory traces. , 1996, Brain : a journal of neurology.

[9]  R. Ptak,et al.  Spontaneous confabulations after Orbitofrontal damage: The role of temporal context confusion and self-monitoring , 1999 .

[10]  D. Joel,et al.  The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum , 2000, Neuroscience.

[11]  Ken A. Paller,et al.  Frontal Brain Potentials during Recognition Are Modulated by Requirements to Retrieve Perceptual Detail , 1999, Neuron.

[12]  E. Rolls,et al.  The Orbitofrontal Cortex , 2019 .

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

[14]  Christoph M. Michel,et al.  Early Cortical Distinction between Memories that Pertain to Ongoing Reality and Memories that Don't , 2002 .

[15]  Valerie Treyer,et al.  Selection of Currently Relevant Memories by the Human Posterior Medial Orbitofrontal Cortex , 2000, The Journal of Neuroscience.

[16]  A. Schnider Commentary on “The Pleasantness of False Beliefs” , 2004 .

[17]  Marcia K. Johnson,et al.  Left Anterior Prefrontal Activation Increases with Demands to Recall Specific Perceptual Information , 2000, The Journal of Neuroscience.

[18]  M. Rugg,et al.  Context Effects on the Neural Correlates of Recognition Memory An Electrophysiological Study , 2001, Neuron.

[19]  E. Crosby,et al.  Korsakoff's syndrome associated with surgical lesions involving the mammillary bodies , 1972, Neurology.

[20]  Marcia K. Johnson,et al.  Left prefrontal activation during episodic remembering: an event‐related fMRI study , 1998, Neuroreport.

[21]  J. DeLuca,et al.  Confabulation Following Aneurysm of the Anterior Communicating Artery , 1991, Cortex.

[22]  E. Renzi,et al.  Bilateral paramedian thalamic artery infarcts: report of eight cases. , 1987, Journal of neurology, neurosurgery, and psychiatry.

[23]  N. Valenza,et al.  Early cortical distinction between memories that pertain to ongoing reality and memories that do not , 2001, NeuroImage.

[24]  Daniel L. Schacter,et al.  The Cognitive Neuroscience of Memory Distortion , 2004, Neuron.

[25]  Paul W. Burgess,et al.  Content-Specific Confabulation , 1999, Cortex.

[26]  Marcia K. Johnson,et al.  Source monitoring. , 1993, Psychological bulletin.

[27]  Armin Schnider,et al.  Spontaneous confabulation, reality monitoring, and the limbic system — a review , 2001, Brain Research Reviews.

[28]  D Friedman,et al.  Cognitive event-related potential components during continuous recognition memory for pictures. , 1990, Psychophysiology.

[29]  N. Stanhope,et al.  Temporal and spatial context memory in patients with focal frontal, temporal lobe, and diencephalic lesions , 1997, Neuropsychologia.

[30]  Arthur P. Shimamura,et al.  Memory for the temporal order of events in patients with frontal lobe lesions and amnesic patients , 1990, Neuropsychologia.

[31]  R. Ptak,et al.  Recovery from spontaneous confabulations parallels recovery of temporal confusion in memory , 2000, Neurology.

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

[33]  Gabriel Leonard,et al.  Frontal-lobe contribution to recency judgements , 1991, Neuropsychologia.

[34]  Joaquin M. Fuster,et al.  Single cell activity in ventral prefrontal cortex of behaving monkeys , 1981, Brain Research.

[35]  M Petrides,et al.  Orbitofrontal cortex: A key prefrontal region for encoding information. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[37]  Emily Stern,et al.  Defining the neurocircuitry of borderline personality disorder: Functional neuroimaging approaches , 2005, Development and Psychopathology.

[38]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.

[39]  Michael D. Rugg,et al.  The Role of the Prefrontal Cortex in Recognition Memory and Memory for Source: An fMRI Study , 1999, NeuroImage.

[40]  Raymond P. Kesner,et al.  Item and order dissociation in humans with prefrontal cortex damage , 1994, Neuropsychologia.

[41]  Marcia K. Johnson,et al.  False memories and confabulation , 1998, Trends in Cognitive Sciences.

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

[43]  E. Rolls,et al.  Abstract reward and punishment representations in the human orbitofrontal cortex , 2001, Nature Neuroscience.

[44]  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.

[45]  HighWire Press Philosophical Transactions of the Royal Society of London , 1781, The London Medical Journal.

[46]  Sean A. Spence,et al.  Descartes' Error: Emotion, Reason and the Human Brain , 1995 .

[47]  S. Thorpe,et al.  The orbitofrontal cortex: Neuronal activity in the behaving monkey , 2004, Experimental Brain Research.

[48]  Armin Schnider,et al.  Spontaneous confabulators fail to suppress currently irrelevant memory traces , 1999, Nature Neuroscience.

[49]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[50]  Marcia K. Johnson,et al.  Confabulation, Memory Deficits, and Frontal Dysfunction , 1997, Brain and Cognition.

[51]  R. Ptak,et al.  Hypothalamic amnesia with spontaneous confabulations: A clinicopathologic study , 2001, Neurology.

[52]  G. Percheron,et al.  [Informational analysis of the basal ganglia related system]. , 1994, Revue neurologique.