Dataset Information

Stimulus repetition modulates gamma-band synchronization in primate visual cortex.

ABSTRACT: When a sensory stimulus repeats, neuronal firing rate and functional MRI blood oxygen level-dependent responses typically decline, yet perception and behavioral performance either stay constant or improve. An additional aspect of neuronal activity is neuronal synchronization, which can enhance the impact of neurons onto their postsynaptic targets independent of neuronal firing rates. We show that stimulus repetition leads to profound changes of neuronal gamma-band (?40-90 Hz) synchronization. Electrocorticographic recordings in two awake macaque monkeys demonstrated that repeated presentations of a visual grating stimulus resulted in a steady increase of visually induced gamma-band activity in area V1, gamma-band synchronization between areas V1 and V4, and gamma-band activity in area V4. Microelectrode recordings in area V4 of two additional monkeys under the same stimulation conditions allowed a direct comparison of firing rates and gamma-band synchronization strengths for multiunit activity (MUA), as well as for isolated single units, sorted into putative pyramidal cells and putative interneurons. MUA and putative interneurons showed repetition-related decreases in firing rate, yet increases in gamma-band synchronization. Putative pyramidal cells showed no repetition-related firing rate change, but a decrease in gamma-band synchronization for weakly stimulus-driven units and constant gamma-band synchronization for strongly driven units. We propose that the repetition-related changes in gamma-band synchronization maintain the interareal stimulus signaling and sharpen the stimulus representation by gamma-synchronized pyramidal cell spikes.

SUBMITTER: Brunet NM

PROVIDER: S-EPMC3948273 | biostudies-literature | 2014 Mar

REPOSITORIES: biostudies-literature

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Stimulus repetition modulates gamma-band synchronization in primate visual cortex.

Brunet Nicolas M NM Bosman Conrado A CA Vinck Martin M Roberts Mark M Oostenveld Robert R Desimone Robert R De Weerd Peter P Fries Pascal P

Proceedings of the National Academy of Sciences of the United States of America 20140219 9

When a sensory stimulus repeats, neuronal firing rate and functional MRI blood oxygen level-dependent responses typically decline, yet perception and behavioral performance either stay constant or improve. An additional aspect of neuronal activity is neuronal synchronization, which can enhance the impact of neurons onto their postsynaptic targets independent of neuronal firing rates. We show that stimulus repetition leads to profound changes of neuronal gamma-band (∼40-90 Hz) synchronization. El ...[more]

PMID: 24554080

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Project description:Similar to primates, visual cortex in rodents appears to be organized in two distinct hierarchical streams. However, there is still little known about how visual information is processed along those streams in rodents. In this study, we examined how repetition suppression and position and clutter tolerance of the neuronal representations evolve along the putative ventral visual stream in rats. To address this question, we recorded multiunit spiking activity in primary visual cortex (V1) and the more downstream visual laterointermediate (LI) area of head-restrained Long-Evans rats. We employed a paradigm reminiscent of the continuous carry-over design used in human neuroimaging. In both areas, stimulus repetition attenuated the early phase of the neuronal response to the repeated stimulus, with this response suppression being greater in area LI. Furthermore, stimulus preferences were more similar across positions (position tolerance) in area LI than in V1, even though the absolute responses in both areas were very sensitive to changes in position. In contrast, the neuronal representations in both areas were equally good at tolerating the presence of limited visual clutter, as modeled by the presentation of a single flank stimulus. When probing tolerance of the neuronal representations with stimulus-specific adaptation, we detected no position tolerance in either examined brain area, whereas, on the contrary, we revealed clutter tolerance in both areas. Overall, our data demonstrate similarities and discrepancies in processing of visual information along the ventral visual stream of rodents and primates. Moreover, our results stress caution in using neuronal adaptation to probe tolerance of the neuronal representations. NEW & NOTEWORTHY Rodents are emerging as a popular animal model that complement primates for studying higher level visual functions. Similar to findings in primates, we demonstrate a greater repetition suppression and position tolerance of the neuronal representations in the downstream laterointermediate area of Long-Evans rats compared with primary visual cortex. However, we report no difference in the degree of clutter tolerance between the areas. These findings provide additional evidence for hierarchical processing of visual stimuli in rodents.

Dataset Information

Stimulus repetition modulates gamma-band synchronization in primate visual cortex.

Publications

Stimulus repetition modulates gamma-band synchronization in primate visual cortex.

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