Temporal Dynamics of Neural Adaptation Effect in the Human Visual Ventral Stream

When the same visual stimulus is repeatedly presented with a brief interval, the brain responses to that stimulus are attenuated relative to those at first presentation [neural adaptation (NA)]. Although this effect has been widely observed in various regions of human brain, its temporal dynamics as a neuronal population has been mostly unclear. In the present study, we used a magnetoencephalography (MEG) and conducted a macrolevel investigation of the temporal profiles of the NA occurring in the human visual ventral stream. The combination of MEG with our previous random dot blinking method isolated the neural responses in the higher visual cortex relating to shape perception. We dissociated three dimensions of the NA: activation strength, peak latency, and temporal duration of neural response. The results revealed that visual responses to the repeated compared with novel stimulus showed a significant reduction in both activation strength and peak latency but not in the duration of neural processing. Furthermore, this acceleration of peak latency showed a significant correlation with reaction time of the subjects, whereas no correlation was found between the reaction time and the temporal duration of neural responses. These results indicate that (1) the NA involves the brain response changes in the temporal domain as well as the response attenuation reported previously, and (2) this temporal change is primarily observed as a rapid rising of “what” responses, rather than a temporal shortening of neural response curves within the visual ventral stream as considered previously.

[1]  S. Becker,et al.  Long-term semantic priming: a computational account and empirical evidence. , 1997, Journal of experimental psychology. Learning, memory, and cognition.

[2]  R. Turner,et al.  Detecting Latency Differences in Event-Related BOLD Responses: Application to Words versus Nonwords and Initial versus Repeated Face Presentations , 2002, NeuroImage.

[3]  G. R. Mangun,et al.  Form-From-Motion: MEG Evidence for Time Course and Processing Sequence , 2003, Journal of Cognitive Neuroscience.

[4]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[5]  Irene P. Kan,et al.  Effects of Repetition and Competition on Activity in Left Prefrontal Cortex during Word Generation , 1999, Neuron.

[6]  S. Petersen,et al.  Practice-related changes in human brain functional anatomy during nonmotor learning. , 1994, Cerebral cortex.

[7]  T. Allison,et al.  Electrophysiological studies of human face perception. III: Effects of top-down processing on face-specific potentials. , 1999, Cerebral cortex.

[8]  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.

[9]  Alex Martin,et al.  Long-lasting cortical plasticity in the object naming system , 2000, Nature Neuroscience.

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

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

[12]  N. Kanwisher,et al.  Cortical Regions Involved in Perceiving Object Shape , 2000, The Journal of Neuroscience.

[13]  T. Shallice,et al.  Face repetition effects in implicit and explicit memory tests as measured by fMRI. , 2002, Cerebral cortex.

[14]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[15]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[16]  T. Shallice,et al.  Neuroimaging evidence for dissociable forms of repetition priming. , 2000, Science.

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

[18]  Hiroki Nakata,et al.  Gating of somatosensory evoked magnetic fields during the preparatory period of self-initiated finger movement , 2003, NeuroImage.

[19]  S. Hillyard,et al.  Delayed Striate Cortical Activation during Spatial Attention , 2002, Neuron.

[20]  R. Kakigi,et al.  Random dots blinking: a new approach to elucidate the activities of the extrastriate cortex in humans , 1998, Neuroreport.

[21]  D. Schacter,et al.  Task-specific repetition priming in left inferior prefrontal cortex. , 2000, Cerebral cortex.

[22]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[23]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

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

[25]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

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

[27]  S. Dehaene,et al.  The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. , 2001, Cerebral cortex.

[28]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

[29]  A. Dale,et al.  Functional-Anatomic Correlates of Object Priming in Humans Revealed by Rapid Presentation Event-Related fMRI , 1998, Neuron.

[30]  Eric Halgren,et al.  Cortical activation to illusory shapes as measured with magnetoencephalography , 2003, NeuroImage.

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

[32]  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.

[33]  R L Buckner,et al.  Spatiotemporal Maps of Brain Activity Underlying Word Generation and Their Modification during Repetition Priming , 2001, The Journal of Neuroscience.

[34]  Valerie A. Carr,et al.  Spatiotemporal Dynamics of Modality-Specific and Supramodal Word Processing , 2003, Neuron.