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      Selectivity of Neuromodulatory Projections from the Basal Forebrain and Locus Ceruleus to Primary Sensory Cortices

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          Abstract

          Acetylcholine and noradrenaline are major neuromodulators that affect sensory processing in the cortex. Modality-specific sensory information is processed in defined areas of the cortex, but it is unclear whether cholinergic neurons in the basal forebrain (BF) and noradrenergic neurons in the locus ceruleus (LC) project to and modulate these areas in a sensory modality-selective manner. Here, we mapped BF and LC projections to different sensory cortices of the mouse using dual retrograde tracing. We found that while the innervation of cholinergic neurons into sensory cortices is predominantly modality specific, the projections of noradrenergic neurons diverge onto multiple sensory cortices. Consistent with this anatomy, optogenetic activation of cholinergic neurons in BF subnuclei induces modality-selective desynchronization in specific sensory cortices, whereas activation of noradrenergic LC neurons induces broad desynchronization throughout multiple sensory cortices. Thus, we demonstrate a clear distinction in the organization and function of cholinergic BF and noradrenergic LC projections into primary sensory cortices: cholinergic BF neurons are highly selective in their projections and modulation of specific sensory cortices, whereas noradrenergic LC neurons broadly innervate and modulate multiple sensory cortices.

          SIGNIFICANCE STATEMENT Neuromodulatory inputs from the basal forebrain (BF) and locus ceruleus (LC) are widespread in the mammalian cerebral cortex and are known to play important roles in attention and arousal, but little is known about the selectivity of their cortical projections. Using a dual retrobead tracing technique along with optogenetic stimulation, we have identified anatomic and functional differences in the way cholinergic BF neurons and noradrenergic LC neurons project into primary sensory cortices. While BF projections are highly selective to individual sensory cortices, LC projections diverge into multiple sensory cortices. To our knowledge, this is the first definitive proof that BF and LC projections to primary sensory cortices show both anatomic and functional differences in selectivity for modulating cortical activity.

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          Author and article information

          Journal
          J Neurosci
          J. Neurosci
          jneuro
          jneurosci
          J. Neurosci
          The Journal of Neuroscience
          Society for Neuroscience
          0270-6474
          1529-2401
          11 May 2016
          : 36
          : 19
          : 5314-5327
          Affiliations
          1Department of Biological Sciences, Korea Advanced Institute of Science and Technology, Daejeon 34141, Korea, and
          2Department of Electrical and Computer Engineering, Seoul National University, Seoul 08826, Korea
          Author notes
          Correspondence should be addressed to Seung-Hee Lee at the above address. shlee1@ 123456kaist.ac.kr

          Author contributions: J.-H.K. and S.-H.L. designed research; J.-H.K., A.-H.J., D.J., and S.-H.L. performed research; S.S. and S.J.K. contributed unpublished reagents/analytic tools; A.-H.J., I.C., and K.K. analyzed data; J.-H.K. and S.-H.L. wrote the paper.

          Article
          PMC6601800 PMC6601800 6601800 4333-15
          10.1523/JNEUROSCI.4333-15.2016
          6601800
          27170128
          Copyright © 2016 the authors 0270-6474/16/365314-14$15.00/0
          Categories
          Articles
          Systems/Circuits

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