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Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex

Nature Neuroscience volume 13, pages 1011–1019 (2010)Cite this article

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Abstract

Top-down signals from frontal cortex are thought to be important in cognitive control of sensory processing. To explore this interaction, we compared activity in ferret frontal cortex and primary auditory cortex (A1) during auditory and visual tasks requiring discrimination between classes of reference and target stimuli. Frontal cortex responses were behaviorally gated, selectively encoded the timing and invariant behavioral meaning of target stimuli, could be rapid in onset, and sometimes persisted for hours following behavior. These results are consistent with earlier findings in A1 that attention triggered rapid, selective, persistent, task-related changes in spectrotemporal receptive fields. Simultaneously recorded local field potentials revealed behaviorally gated changes in inter-areal coherence that were selectively modulated between frontal cortex and focal regions of A1 that were responsive to target sounds. These results suggest that A1 and frontal cortex dynamically establish a functional connection during auditory behavior that shapes the flow of sensory information and maintains a persistent trace of recent task-relevant stimulus features.

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Figure 1: Sites of physiological recordings.
Figure 2: Behavioral procedure and examples of typical frontal cortex neuron responses.
Figure 3: Frontal cortex population target responses during tone-detection behavior.
Figure 4: Frontal cortex class-specific responses to task-relevant sounds.
Figure 5: Persistence and extinction of frontal cortex responses following behavior.
Figure 6: Selective top-down modulation of LFP in A1 and frontal cortex.
Figure 7: Bimodal and unimodal sensory responses in frontal cortex.

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Acknowledgements

We would like to thank A. Duque, J. Bizley, V. Bajo, F. Nodal and A. King for discussion and for generously sharing their unpublished neuroanatomical data on the ferret frontal cortex and its connectivity with auditory cortex, N. Mesgarani for assistance with customized MATLAB software development, M. Elhilali for discussion and for analysis of memory effects in A1, S. Gotts for discussion of LFP coherence, C. Carr for cheerfully sharing laboratory resources for neuroanatomical studies and A. Israelson, A. Rubin, K. Donaldson and D. Levitt for assistance in training the ferrets in this study. This research was funded by grants from the US National Institutes of Health (R03DC005938 to J.B.F., R01DC005779 to S.A.S. and J.B.F. and F32DC008453 to S.V.D.).

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Authors and Affiliations

  1. Institute for Systems Research, University of Maryland, College Park, Maryland, USA

    Jonathan B Fritz, Stephen V David, Pingbo Yin & Shihab A Shamma

  2. Division of Neurobiology, Biocenter of Ludwig Maximilians University, Munich, Germany

    Susanne Radtke-Schuller

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  1. Jonathan B Fritz
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Contributions

J.B.F. designed and conducted all behavioral physiological experiments. S.V.D. analyzed data. J.B.F., S.V.D. and S.A.S. evaluated results. J.B.F. and P.Y. made neuroanatomical tracer injections. S.R.-S. processed all histological tissue, analyzed neuroanatomical results and made one figure. S.V.D. made all other figures. J.B.F., S.A.S. and S.V.D. wrote the manuscript.

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Correspondence to Jonathan B Fritz.

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Fritz, J., David, S., Radtke-Schuller, S. et al. Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat Neurosci 13, 1011–1019 (2010). https://doi.org/10.1038/nn.2598

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