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Cross-modal and cross-temporal association in neurons of frontal cortex

Abstract

The prefrontal cortex is essential for the temporal integration of sensory information in behavioural and linguistic sequences1,2. Such information is commonly encoded in more than one sense modality, notably sight and sound. Connections from sensory cortices to the prefrontal cortex support its integrative function3,4,5. Here we present the first evidence that prefrontal cortex cells associate visual and auditory stimuli across time. We gave monkeys the task of remembering a tone of a certain pitch for 10 s and then choosing the colour associated with it. In this task, prefrontal cortex cells responded selectively to tones, and most of them also responded to colours according to the task rule. Thus, their reaction to a tone was correlated with their subsequent reaction to the associated colour. This correlation faltered in trials ending in behavioural error. We conclude that prefrontal cortex neurons are part of integrative networks that represent behaviourally meaningful cross-modal associations. The orderly and timely activation of neurons in such networks is crucial for the temporal transfer of information in the structuring of behaviour, reasoning and language.

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Figure 1: Sound–colour matching task.
Figure 2: Whole-trial activity of three low-tone selective cells.
Figure 3: Firing-frequency histograms from ten prefrontal units showing behavioural concordance of firing at tones (first second of tone) and colours (last second of colour).
Figure 4: Behaviourally concordant correlations between cell responses to tones and colours.

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Acknowledgements

We thank W. Bergerson and B. Lubell for technical assistance; L. Fairbanks for statistical counsel; and C. R. Gallistel, J. Maunsell, W. T. Newsome, T. Sejnowski and Y. Zhou for valuable comments on the manuscript. This work was supported by grants from the National Institute of Mental Health.

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Correspondence to Joaquín M. Fuster.

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Fuster, J., Bodner, M. & Kroger, J. Cross-modal and cross-temporal association in neurons of frontal cortex . Nature 405, 347–351 (2000). https://doi.org/10.1038/35012613

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