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Basal forebrain activation enhances cortical coding of natural scenes

Abstract

The nucleus basalis of the basal forebrain is an essential component of the neuromodulatory system controlling the behavioral state of an animal and it is thought to be important in regulating arousal and attention. However, the effect of nucleus basalis activation on sensory processing remains poorly understood. Using polytrode recording in rat visual cortex, we found that nucleus basalis stimulation caused prominent decorrelation between neurons and marked improvement in the reliability of neuronal responses to natural scenes. The decorrelation depended on local activation of cortical muscarinic acetylcholine receptors, whereas the increased reliability involved distributed neural circuits, as evidenced by nucleus basalis–induced changes in thalamic responses. Further analysis showed that the decorrelation and increased reliability improved cortical representation of natural stimuli in a complementary manner. Thus, the basal forebrain neuromodulatory circuit, which is known to be activated during aroused and attentive states, acts through both local and distributed mechanisms to improve sensory coding.

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Figure 1: Effects of nucleus basalis stimulation on local field activity in V1.
Figure 2: Effect of nucleus basalis stimulation on multiunit activity throughout the depth of cortex.
Figure 3: Nucleus basalis stimulation decreases correlation between cortical neurons during visual stimulation.
Figure 4: Nucleus basalis stimulation increases the reliability of individual neurons in response to natural scenes.
Figure 5: Application of mAChR antagonist diminishes nucleus basalis-induced decorrelation, but does not affect increases in response reliability.
Figure 6: Nucleus basalis stimulation increases response reliability and shifts firing mode in the LGN.
Figure 7: Increased reliability and decreased correlation both contribute to improved coding of natural stimuli.

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Acknowledgements

We thank T. Blanche, D. Feldman, R. Froemke, D. Jones, D. Kleinfeld, C. Niell and A. Vahidnia for technical help and useful discussions. This work was supported by grants from the US National Institutes of Health to Y.D. and a Ruth L. Kirschstein National Research Service Award to M.G. (award number F31NS059258 from the US National Institute of Neurological Disorders and Stroke).

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M.G. conducted all of the experiments. M.G. and Y.D. designed the experiments and wrote the manuscript.

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Correspondence to Yang Dan.

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Goard, M., Dan, Y. Basal forebrain activation enhances cortical coding of natural scenes. Nat Neurosci 12, 1444–1449 (2009). https://doi.org/10.1038/nn.2402

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