Mirror neurons in monkey area F5 do not adapt to the observation of repeated actions

Repetitive presentation of the same visual stimulus entails a response decrease in the action potential discharge of neurons in various areas of the monkey visual cortex. It is still unclear whether this repetition suppression effect is also present in single neurons in cortical premotor areas responding to visual stimuli, as suggested by the human functional magnetic resonance imaging literature. Here we report the responses of 'mirror neurons' in monkey area F5 to the repeated presentation of action movies. We find that most single neurons and the population at large do not show a significant decrease of the firing rate. On the other hand, simultaneously recorded local field potentials exhibit repetition suppression. As local field potentials are believed to be better linked to the blood-oxygen-level-dependent (BOLD) signal exploited by functional magnetic resonance imaging, these findings suggest caution when trying to derive conclusions on the spiking activity of neurons in a given area based on the observation of BOLD repetition suppression.

[1]  Michael J. Constantino,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008 .

[2]  Karl J. Friston,et al.  Evidence of Mirror Neurons in Human Inferior Frontal Gyrus , 2009, The Journal of Neuroscience.

[3]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[4]  D. Heeger,et al.  Normal Movement Selectivity in Autism , 2010, Neuron.

[5]  Nikolaus Weiskopf,et al.  Dissociable roles of human inferior frontal gyrus during action execution and observation , 2012, NeuroImage.

[6]  J. Ringo,et al.  Investigation of long term recognition and association memory in unit responses from inferotemporal cortex , 1993, Experimental Brain Research.

[7]  M. W. Brown,et al.  Neuronal evidence that inferomedial temporal cortex is more important than hippocampus in certain processes underlying recognition memory , 1987, Brain Research.

[8]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[9]  Scott T. Grafton,et al.  Action outcomes are represented in human inferior frontoparietal cortex. , 2008, Cerebral cortex.

[10]  A. Kohn Visual adaptation: physiology, mechanisms, and functional benefits. , 2007, Journal of neurophysiology.

[11]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[12]  S. Schanberg,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 2005 .

[13]  Joris Vangeneugden,et al.  Stimulus Similarity-Contingent Neural Adaptation Can Be Time and Cortical Area Dependent , 2008, The Journal of Neuroscience.

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

[15]  E. Rolls,et al.  Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks , 2004, Experimental Brain Research.

[16]  G. Orban,et al.  How task-related are the responses of inferior temporal neurons? , 1995, Visual Neuroscience.

[17]  Georgios A Keliris,et al.  Neurons in macaque area V4 acquire directional tuning after adaptation to motion stimuli , 2005, Nature Neuroscience.

[18]  J. Movshon,et al.  Neuronal Adaptation to Visual Motion in Area MT of the Macaque , 2003, Neuron.

[19]  Ehud Zohary,et al.  Dissociation between Ventral and Dorsal fMRI Activation during Object and Action Recognition , 2005, Neuron.

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

[21]  Alfonso Caramazza,et al.  Asymmetric fMRI adaptation reveals no evidence for mirror neurons in humans , 2009, Proceedings of the National Academy of Sciences.

[22]  G. Rizzolatti,et al.  Mirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys , 2009, Science.

[23]  J. Ringo Stimulus specific adaptation in inferior temporal and medial temporal cortex of the monkey , 1996, Behavioural Brain Research.

[24]  R. Desimone,et al.  A neural mechanism for working and recognition memory in inferior temporal cortex. , 1991, Science.

[25]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

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

[27]  R. Vogels,et al.  Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. , 2010, Cerebral cortex.

[28]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[29]  Andreas Bartels,et al.  fMRI and its interpretations: an illustration on directional selectivity in area V5/MT , 2008, Trends in Neurosciences.

[30]  E. Miller,et al.  Prospective Coding for Objects in Primate Prefrontal Cortex , 1999, The Journal of Neuroscience.

[31]  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.

[32]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[33]  R. Freeman,et al.  Neurometabolic coupling in cerebral cortex reflects synaptic more than spiking activity , 2007, Nature Neuroscience.

[34]  G. Rizzolatti,et al.  Action recognition in the premotor cortex. , 1996, Brain : a journal of neurology.

[35]  G L Gerstein,et al.  Single-unit activity in temporal association cortex of the monkey. , 1967, Journal of neurophysiology.

[36]  T. Pasternak,et al.  Directional Signals in the Prefrontal Cortex and in Area MT during a Working Memory for Visual Motion Task , 2006, The Journal of Neuroscience.

[37]  D I Perrett,et al.  Frameworks of analysis for the neural representation of animate objects and actions. , 1989, The Journal of experimental biology.

[38]  G. Orban,et al.  Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm , 2006, Neuron.

[39]  G. Rizzolatti,et al.  View-Based Encoding of Actions in Mirror Neurons of Area F5 in Macaque Premotor Cortex , 2011, Current Biology.

[40]  T. Powell,et al.  A qualitative and quantitative electron microscopic study of the neurons in the primate motor and somatic sensory cortices. , 1979, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[41]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[42]  N. Kanwisher,et al.  fMRI Adaptation Reveals Mirror Neurons in Human Inferior Parietal Cortex , 2008, Current Biology.

[43]  Arno C. Schmitt,et al.  Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A , 2011, Proceedings of the National Academy of Sciences.

[44]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

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

[46]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[47]  Nava Rubin,et al.  Brain areas selective for both observed and executed movements. , 2007, Journal of neurophysiology.

[48]  C. Summerfield,et al.  A Neural Representation of Prior Information during Perceptual Inference , 2008, Neuron.

[49]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[50]  M. W. Brown,et al.  Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex , 2004, Experimental Brain Research.

[51]  E. Miller,et al.  Habituation-like decrease in the responses of neurons in inferior temporal cortex of the macaque , 1991, Visual Neuroscience.