The relationship between stimulus repetitions and fulfilled expectations

Several neuroimaging studies showed that fulfilled expectations increase the magnitude of repetition suppression (RS) in the face-selective visual cortex. However, previous fMRI studies did not allow a distinction between the reductions of the response due to stimulus repetitions and fulfilled expectations (expectation suppression, ES). In most prior studies repetitions and expectations were not independent from each other as repetitions occurred more often when they were expected and less often when they were not expected, thereby confounding RS with ES. To overcome this confound, we presented pairs of female and male faces that were either repeating or alternating with an overall probability of 50-50%. Orthogonally to this, the gender of the first face in each pair signaled with 75% accuracy whether repetitions or alternations were more likely to occur. We found significant RS in the FFA, the OFA and the LO. In addition, these areas showed a reduction of the response for expected when compared to surprising trials. Moreover, the effects of RS and ES were always additive rather than interactive in our ROIs. This implies that stimulus repetition and fulfilled expectations can be dissociated from one another in terms of their effects on the neural responses.

[1]  Nancy Kanwisher,et al.  fMRI evidence for objects as the units of attentional selection , 1999, Nature.

[2]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[3]  Karl J. Friston,et al.  A Dual Role for Prediction Error in Associative Learning , 2008, Cerebral cortex.

[4]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[5]  R. Henson,et al.  Explaining away repetition effects via predictive coding , 2012, Cognitive neuroscience.

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

[7]  G. Kovács,et al.  Neural correlates of high-level adaptation-related aftereffects. , 2010, Journal of neurophysiology.

[8]  Vanessa M. Johnen,et al.  Human Scalp Electroencephalography Reveals that Repetition Suppression Varies with Expectation , 2011, Front. Hum. Neurosci..

[9]  Jim M. Monti,et al.  Expectation and Surprise Determine Neural Population Responses in the Ventral Visual Stream , 2010, The Journal of Neuroscience.

[10]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[11]  A. Horner,et al.  Focusing on the frontal cortex , 2012, Cognitive neuroscience.

[12]  Jennifer A. Mangels,et al.  Predictive Codes for Forthcoming Perception in the Frontal Cortex , 2006, Science.

[13]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[14]  Caspar M. Schwiedrzik,et al.  Stimulus Predictability Reduces Responses in Primary Visual Cortex , 2010, The Journal of Neuroscience.

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

[16]  Mark W. Greenlee,et al.  Stimulus repetition probability effects on repetition suppression are position invariant for faces , 2012, NeuroImage.

[17]  Jonas Larsson,et al.  fMRI repetition suppression: neuronal adaptation or stimulus expectation? , 2012, Cerebral cortex.

[18]  Mareike Grotheer,et al.  Repetition Probability Effects Depend on Prior Experiences , 2014, The Journal of Neuroscience.

[19]  C. Olson,et al.  Statistical learning of visual transitions in monkey inferotemporal cortex , 2011, Proceedings of the National Academy of Sciences.

[20]  R. Henson Neuroimaging studies of priming , 2003, Progress in Neurobiology.

[21]  Rufin Vogels,et al.  Stimulus repetition probability does not affect repetition suppression in macaque inferior temporal cortex. , 2011, Cerebral cortex.

[22]  C. Summerfield,et al.  Attention Sharpens the Distinction between Expected and Unexpected Percepts in the Visual Brain , 2013, The Journal of Neuroscience.

[23]  Rafael Malach,et al.  Targeting the functional properties of cortical neurons using fMR-adaptation , 2012, NeuroImage.

[24]  Mareike Grotheer,et al.  Repetition probability effects for inverted faces , 2014, NeuroImage.

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

[26]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[27]  R. Vogels,et al.  Repetition Probability Does Not Affect fMRI Repetition Suppression for Objects , 2013, The Journal of Neuroscience.

[28]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[29]  A. Todorović,et al.  Repetition Suppression and Expectation Suppression Are Dissociable in Time in Early Auditory Evoked Fields , 2012, The Journal of Neuroscience.

[30]  S. Dehaene,et al.  Evidence for a hierarchy of predictions and prediction errors in human cortex , 2011, Proceedings of the National Academy of Sciences.

[31]  I. Johnsrude,et al.  The problem of functional localization in the human brain , 2002, Nature Reviews Neuroscience.

[32]  Martin Kronbichler,et al.  Neural repetition suppression: evidence for perceptual expectation in object-selective regions , 2014, Front. Hum. Neurosci..

[33]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[34]  Rufin Vogels,et al.  When does repetition suppression depend on repetition probability? , 2014, Front. Hum. Neurosci..

[35]  Scott T. Grafton,et al.  Reductions in neural activity underlie behavioral components of repetition priming , 2005, Nature Neuroscience.

[36]  Lora T. Likova,et al.  The Neurometabolic Underpinnings of fMRI BOLD Dynamics , 2014 .

[37]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .