The Effect of Attention on Repetition Suppression and Multivoxel Pattern Similarity

Fundamental to our understanding of learning is the role of attention. We investigated how attention affects two fMRI measures of stimulus-specific memory: repetition suppression (RS) and pattern similarity (PS). RS refers to the decreased fMRI signal when a stimulus is repeated, and it is sensitive to manipulations of attention and task demands. In PS, region-wide voxel-level patterns of responses are evaluated for their similarity across repeated presentations of a stimulus. More similarity across presentations is related to better learning, but the role of attention on PS is not known. Here, we directly compared these measures during the visual repetition of scenes while manipulating attention. Consistent with previous findings, we observed RS in the scene-sensitive parahippocampal place area only when a scene was attended both at initial presentation and upon repetition in subsequent trials, indicating that attention is important for RS. Likewise, we observed greater PS in response to repeated pairs of scenes when both instances of the scene were attended than when either or both were ignored. However, RS and PS did not correlate on either a scene-by-scene or subject-by-subject basis, and PS measures revealed above-chance similarity even when stimuli were ignored. Thus, attention has different effects on RS and PS measures of perceptual repetition.

[1]  Leslie G. Ungerleider,et al.  Repetition suppression of faces is modulated by emotion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[2]  R. Buckner,et al.  Evidence for Neural Effects of Repetition that Directly Correlate with Behavioral Priming , 2004, Journal of Cognitive Neuroscience.

[3]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[4]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[5]  Adler J. Perotte,et al.  Methods for reducing interference in the Complementary Learning Systems model: Oscillating inhibition and autonomous memory rehearsal , 2005, Neural Networks.

[6]  N. Kanwisher,et al.  Visual attention: Insights from brain imaging , 2000, Nature Reviews Neuroscience.

[7]  Marcia K. Johnson,et al.  Memory: Enduring Traces of Perceptual and Reflective Attention , 2011, Neuron.

[8]  Wesley T. Kerr,et al.  Distinguishing conjoint and independent neural tuning for stimulus features with fMRI adaptation. , 2009, Journal of neurophysiology.

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

[10]  W. Greenough,et al.  Experience and brain development. , 1987, Child development.

[11]  Brice A. Kuhl,et al.  Repetition Suppression and Multi-Voxel Pattern Similarity Differentially Track Implicit and Explicit Visual Memory , 2013, The Journal of Neuroscience.

[12]  Richard L. Lewis,et al.  The mind and brain of short-term memory. , 2008, Annual review of psychology.

[13]  Russell A. Epstein,et al.  Neural responses to visual scenes reveals inconsistencies between fMRI adaptation and multivoxel pattern analysis , 2012, Neuropsychologia.

[14]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[15]  G. Aguirre,et al.  Different spatial scales of shape similarity representation in lateral and ventral LOC. , 2009, Cerebral cortex.

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

[17]  M. Chun,et al.  Linking Implicit and Explicit Memory: Common Encoding Factors and Shared Representations , 2006, Neuron.

[18]  Lila Davachi,et al.  Similarity Breeds Proximity: Pattern Similarity within and across Contexts Is Related to Later Mnemonic Judgments of Temporal Proximity , 2014, Neuron.

[19]  R. Henson,et al.  Neural response suppression, haemodynamic repetition effects, and behavioural priming , 2003, Neuropsychologia.

[20]  Kenneth A. Norman,et al.  Recollection, Familiarity, and Cortical Reinstatement: A Multivoxel Pattern Analysis , 2009, Neuron.

[21]  J. Mumford,et al.  Greater Neural Pattern Similarity Across Repetitions Is Associated with Better Memory , 2010, Science.

[22]  Edward F. Ester,et al.  PSYCHOLOGICAL SCIENCE Research Article Stimulus-Specific Delay Activity in Human Primary Visual Cortex , 2022 .

[23]  Brice A. Kuhl,et al.  Fidelity of neural reactivation reveals competition between memories , 2011, Proceedings of the National Academy of Sciences.

[24]  R. Henson,et al.  BOLD repetition decreases in object-responsive ventral visual areas depend on spatial attention. , 2004, Journal of neurophysiology.

[25]  M. Chun,et al.  Attentional Modulation of Learning-Related Repetition Attenuation Effects in Human Parahippocampal Cortex , 2005, The Journal of Neuroscience.

[26]  M. Chun,et al.  Interactions between attention and memory , 2007, Current Opinion in Neurobiology.

[27]  Denis Schluppeck,et al.  A comparison of fMRI adaptation and multivariate pattern classification analysis in visual cortex , 2010, NeuroImage.

[28]  J. Ringo,et al.  Mnemonic Responses of Single Units Recorded from Monkey Inferotemporal Cortex, Accessed via Transcommissural Versus Direct Pathways: A Dissociation between Unit Activity and Behavior , 1996, The Journal of Neuroscience.

[29]  Marcia K. Johnson,et al.  Top–Down Enhancement and Suppression of Activity in Category-selective Extrastriate Cortex from an Act of Reflective Attention , 2009, Journal of Cognitive Neuroscience.

[30]  G. Xue,et al.  Spatiotemporal Neural Pattern Similarity Supports Episodic Memory , 2015, Current Biology.

[31]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[32]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[33]  Sean M. Polyn,et al.  Beyond mind-reading: multi-voxel pattern analysis of fMRI data , 2006, Trends in Cognitive Sciences.

[34]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[35]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[36]  Jarmo A. Hämäläinen,et al.  Repetition suppression comprises both attention-independent and attention-dependent processes , 2014, NeuroImage.

[37]  J. Movshon,et al.  Adaptation changes the direction tuning of macaque MT neurons , 2004, Nature Neuroscience.

[38]  R. Desimone,et al.  Inferior temporal mechanisms for invariant object recognition. , 1994, Cerebral cortex.