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Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance

Abstract

Short-term memory requires communication between multiple brain regions that collectively mediate the encoding and maintenance of sensory information. It has been suggested that oscillatory synchronization underlies intercortical communication. Yet, whether and how distant cortical areas cooperate during visual memory remains elusive. We examined neural interactions between visual area V4 and the lateral prefrontal cortex using simultaneous local field potential (LFP) recordings and single-unit activity (SUA) in monkeys performing a visual short-term memory task. During the memory period, we observed enhanced between-area phase synchronization in theta frequencies (3–9 Hz) of LFPs together with elevated phase locking of SUA to theta oscillations across regions. In addition, we found that the strength of intercortical locking was predictive of the animals' behavioral performance. This suggests that theta-band synchronization coordinates action potential communication between V4 and prefrontal cortex that may contribute to the maintenance of visual short-term memories.

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Figure 1: Experimental procedure, behavioral performance and power modulations in areas V4 and lPF during baseline and delay.
Figure 2: Phase locking between V4 and lPF in theta band.
Figure 3: Enhanced intra-area spike-phase locking in theta during delay.
Figure 4: Inter-area theta phase locking of V4 and prefrontal neurons during visual memory.
Figure 5: Theta-phase locking during the delay is higher for correct than for incorrect trials.
Figure 6: Correlation of phase locking with performance across single sessions.

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Acknowledgements

We would like to thank J. Macke for discussions regarding analyses, and T. Mrsic-Flogel and J. Macke for useful comments on the manuscript. We also thank A.-L. Keller for help with histology. S.L. was supported by the Deutsche Forschungsgemeinschaft Sonderforschungsbereich 550 and a doctoral Fellowship of the Max Planck Society. G.M.H. was supported by projects FP7-231267 (“Self-Organized Recurrent Neural Learning for Language Processing”, ORGANIC) and FP7-506778 (Pattern Analysis, Statistical Modeling and Computational Learning, PASCAL2 ) of the European Union. G.R. is a European Science Foundation European Young Investigator.

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S.L. and G.R. designed the experiments. S.L. conducted the experiments. S.L. and G.M.H. analyzed the data. S.L. wrote the manuscript with contributions from G.M.H. and G.R. N.K.L. and G.R. supervised the study.

Corresponding authors

Correspondence to Stefanie Liebe or Gregor Rainer.

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The authors declare no competing financial interests.

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Liebe, S., Hoerzer, G., Logothetis, N. et al. Theta coupling between V4 and prefrontal cortex predicts visual short-term memory performance. Nat Neurosci 15, 456–462 (2012). https://doi.org/10.1038/nn.3038

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