Memory Accumulation Mechanisms in Human Cortex Are Independent of Motor Intentions

Previous studies on perceptual decision-making have often emphasized a tight link between decisions and motor intentions. Human decisions, however, also depend on memories or experiences that are not closely tied to specific motor responses. Recent neuroimaging findings have suggested that, during episodic retrieval, parietal activity reflects the accumulation of evidence for memory decisions. It is currently unknown, however, whether these evidence accumulation signals are functionally linked to signals for motor intentions coded in frontoparietal regions and whether activity in the putative memory accumulator tracks the amount of evidence for only previous experience, as reflected in “old” reports, or for both old and new decisions, as reflected in the accuracy of memory judgments. Here, human participants used saccadic-eye and hand-pointing movements to report recognition judgments on pictures defined by different degrees of evidence for old or new decisions. A set of cortical regions, including the middle intraparietal sulcus, showed a monotonic variation of the fMRI BOLD signal that scaled with perceived memory strength (older > newer), compatible with an asymmetrical memory accumulator. Another set, including the hippocampus and the angular gyrus, showed a nonmonotonic response profile tracking memory accuracy (higher > lower evidence), compatible with a symmetrical accumulator. In contrast, eye and hand effector-specific regions in frontoparietal cortex tracked motor intentions but were not modulated by the amount of evidence for the effector outcome. We conclude that item recognition decisions are supported by a combination of symmetrical and asymmetrical accumulation signals largely segregated from motor intentions.

[1]  M. Corbetta,et al.  Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions , 2008, Nature Neuroscience.

[2]  F. Blankenburg,et al.  Causal Role of Dorsolateral Prefrontal Cortex in Human Perceptual Decision Making , 2011, Current Biology.

[3]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[4]  Martin A. Lindquist,et al.  Detection of time-varying signals in event-related fMRI designs , 2008, NeuroImage.

[5]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[6]  Jeffrey D. Johnson,et al.  Recollection and the reinstatement of encoding-related cortical activity. , 2007, Cerebral cortex.

[7]  Kaia L. Vilberg,et al.  Age differences in the neural correlates of recollection: transient versus sustained fMRI effects , 2012, Neurobiology of Aging.

[8]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[9]  R. Ratcliff,et al.  A Diffusion Model Analysis of the Effects of Aging on Recognition Memory Journal of Memory and Language , 2003 .

[10]  Miranda Robertson,et al.  Neural systems , 1977, Nature.

[11]  M Moscovitch,et al.  Frontal Lobes, Memory, and Aging , 1995, Annals of the New York Academy of Sciences.

[12]  Francis Tuerlinckx,et al.  Fitting the ratcliff diffusion model to experimental data , 2007, Psychonomic bulletin & review.

[13]  Leslie G. Ungerleider,et al.  Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[14]  A. Nobre,et al.  Effects of Decision Variables and Intraparietal Stimulation on Sensorimotor Oscillatory Activity in the Human Brain , 2012, The Journal of Neuroscience.

[15]  C. Galletti,et al.  Brain location and visual topography of cortical area V6A in the macaque monkey , 1999, The European journal of neuroscience.

[16]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[17]  Maurizio Corbetta,et al.  Attention to Memory and the Environment: Functional Specialization and Dynamic Competition in Human Posterior Parietal Cortex , 2010, The Journal of Neuroscience.

[18]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[19]  Julie D. Golomb,et al.  A taxonomy of external and internal attention. , 2011, Annual review of psychology.

[20]  K D Singh,et al.  Transient and linearly graded deactivation of the human default-mode network by a visual detection task , 2008, NeuroImage.

[21]  J. Binder,et al.  A Parametric Manipulation of Factors Affecting Task-induced Deactivation in Functional Neuroimaging , 2003, Journal of Cognitive Neuroscience.

[22]  M. Corbetta,et al.  Episodic Memory Retrieval, Parietal Cortex, and the Default Mode Network: Functional and Topographic Analyses , 2011, The Journal of Neuroscience.

[23]  Roger Ratcliff,et al.  A Theory of Memory Retrieval. , 1978 .

[24]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[25]  R. Cabeza,et al.  Triple dissociation in the medial temporal lobes: recollection, familiarity, and novelty. , 2006, Journal of neurophysiology.

[26]  Timothy F. Brady,et al.  Scene Memory Is More Detailed Than You Think : The Role of Categories in Visual Long-Term Memory , 2010 .

[27]  Adam N. Sanborn,et al.  Model evaluation using grouped or individual data , 2008, Psychonomic bulletin & review.

[28]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[29]  Leslie G. Ungerleider,et al.  The neural systems that mediate human perceptual decision making , 2008, Nature Reviews Neuroscience.

[30]  R. Buckner,et al.  Functional Dissociation among Components of Remembering: Control, Perceived Oldness, and Content , 2003, The Journal of Neuroscience.

[31]  M. Corbetta,et al.  Decision and action planning signals in human posterior parietal cortex during delayed perceptual choices , 2014, The European journal of neuroscience.

[32]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[33]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[34]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[35]  M. Goldberg,et al.  Visual, presaccadic, and cognitive activation of single neurons in monkey lateral intraparietal area. , 1996, Journal of neurophysiology.

[36]  Andreas K. Engel,et al.  Buildup of Choice-Predictive Activity in Human Motor Cortex during Perceptual Decision Making , 2009, Current Biology.

[37]  Scott A. Huettel,et al.  Functional Significance of Striatal Responses during Episodic Decisions: Recovery or Goal Attainment? , 2010, The Journal of Neuroscience.

[38]  J. Gold,et al.  Caudate Encodes Multiple Computations for Perceptual Decisions , 2010, The Journal of Neuroscience.

[39]  Timothy D. Hanks,et al.  Neurobiology of decision making: An intentional framework , 2008 .

[40]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[41]  Maurizio Corbetta,et al.  Interference with episodic memory retrieval following transcranial stimulation of the inferior but not the superior parietal lobule , 2013, Neuropsychologia.

[42]  James L. McClelland,et al.  A Differentiation Account of Recognition Memory: Evidence from fMRI , 2013, Journal of Cognitive Neuroscience.

[43]  Philip L. Smith,et al.  Psychology and neurobiology of simple decisions , 2004, Trends in Neurosciences.

[44]  Jason M. Scimeca,et al.  Striatal Contributions to Declarative Memory Retrieval , 2012, Neuron.

[45]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[46]  Jonathan D. Power,et al.  A Parcellation Scheme for Human Left Lateral Parietal Cortex , 2010, Neuron.

[47]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[48]  David I. Donaldson,et al.  Remember the Source: Dissociating Frontal and Parietal Contributions to Episodic Memory , 2010, Journal of Cognitive Neuroscience.

[49]  M. Moscovitch,et al.  The parietal cortex and episodic memory: an attentional account , 2008, Nature Reviews Neuroscience.

[50]  M. Corbetta,et al.  Common Blood Flow Changes across Visual Tasks: II. Decreases in Cerebral Cortex , 1997, Journal of Cognitive Neuroscience.

[51]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI I. The Method , 2001, NeuroImage.

[52]  Gaspare Galati,et al.  Intentional signals during saccadic and reaching delays in the human posterior parietal cortex , 2011, The European journal of neuroscience.

[53]  Michael B. Miller,et al.  Parietal cortex tracks the amount of information retrieved even when it is not the basis of a memory decision , 2011, NeuroImage.

[54]  Scott D. Brown,et al.  Domain General Mechanisms of Perceptual Decision Making in Human Cortex , 2009, The Journal of Neuroscience.

[55]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

[56]  Kaia L. Vilberg,et al.  Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective , 2008, Neuropsychologia.

[57]  C. Pennartz,et al.  Dissociating the “retrieval success” regions of the brain: Effects of retrieval delay , 2010, Neuropsychologia.

[58]  Francis Tuerlinckx,et al.  Diffusion model analysis with MATLAB: A DMAT primer , 2008, Behavior research methods.

[59]  Kristina M. Visscher,et al.  A Core System for the Implementation of Task Sets , 2006, Neuron.

[60]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[61]  M. D’Esposito,et al.  The functional anatomy of a perceptual decision in the human brain. , 2010, Journal of neurophysiology.

[62]  Melina R. Uncapher,et al.  Functional heterogeneity in posterior parietal cortex across attention and episodic memory retrieval. , 2014, Cerebral cortex.

[63]  E. Rolls A computational theory of episodic memory formation in the hippocampus , 2010, Behavioural Brain Research.

[64]  M. Corbetta,et al.  Separating Processes within a Trial in Event-Related Functional MRI II. Analysis , 2001, NeuroImage.

[65]  Maurizio Corbetta,et al.  Domain-general Signals in the Cingulo-opercular Network for Visuospatial Attention and Episodic Memory , 2014, Journal of Cognitive Neuroscience.

[66]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[67]  K. Duncan,et al.  Memory’s Penumbra: Episodic Memory Decisions Induce Lingering Mnemonic Biases , 2012, Science.

[68]  L. Davachi,et al.  Behavioral/systems/cognitive Functional–neuroanatomic Correlates of Recollection: Implications for Models of Recognition Memory , 2022 .

[69]  I. Dobbins,et al.  Unexpected novelty and familiarity orienting responses in lateral parietal cortex during recognition judgment , 2013, Neuropsychologia.

[70]  Craig E. L. Stark,et al.  When zero is not zero: The problem of ambiguous baseline conditions in fMRI , 2001, Proceedings of the National Academy of Sciences of the United States of America.