Glutamatergic Neurons in the Piriform Cortex Influence the Activity of D1- and D2-Type Receptor-Expressing Olfactory Tubercle Neurons
- Kate A. White1,2,*,
- Yun-Feng Zhang3,*,
- Zhijian Zhang4,*,
- Janardhan P. Bhattarai3,
- Andrew H. Moberly3,
- Estelle E. in 't Zandt1,
- José I. Pena-Bravo1,
- Huijie Mi5,
- Xianglian Jia6,
- Marc V. Fuccillo3,
- Fuqiang Xu4,6,
- Minghong Ma3, and
- Daniel W. Wesson1,2
- 1Department of Pharmacology and Therapeutics, University of Florida, Gainesville, Florida 32610,
- 2Department of Neurosciences, Case Western Reserve University, Cleveland, Ohio 44106,
- 3Department of Neuroscience, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania 19104,
- 4Key Laboratory of Magnetic Resonance in Biological Systems, Wuhan Institute of Physics and Mathematics, Wuhan 430071, P.R. China,
- 5College of Life Sciences, Wuhan University, Wuhan 430072, China, and
- 6Brain Cognition and Brain Disease Institute (BCBDI), Shenzhen Institutes of Advanced Technology, Chinese Academy of Sciences, Shenzhen 518055, China
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Author contributions: K.A.W., Y.-F.Z., Z.Z., J.I.P.B., F.X., M.M., and D.W.W. designed research; K.A.W., Y.-F.Z., Z.Z., J.P.B., A.H.M., E.E.i.t.Z., J.I.P.-B., H.M., X.J., and D.W.W. performed research; K.A.W., Y.-F.Z., Z.Z., J.P.B., A.H.M., E.E.i.t.Z., and M.M. analyzed data; K.A.W. and D.W.W. wrote the first draft of the paper; Y.-F.Z., Z.Z., J.P.B., M.M., and D.W.W. wrote the paper; J.I.P.-B., F.X., M.M., and D.W.W. edited the paper; H.M., X.J., and M.V.F. contributed unpublished reagents/analytic tools.
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↵*K.A.W., Y.-F.Z., and Z.Z. contributed equally to this work.
Abstract
Sensory cortices process stimuli in manners essential for perception. Very little is known regarding interactions between olfactory cortices. The piriform “primary” olfactory cortex, especially its anterior division (aPCX), extends dense association fibers into the ventral striatum's olfactory tubercle (OT), yet whether this corticostriatal pathway is capable of shaping OT activity, including odor-evoked activity, is unknown. Further unresolved is the synaptic circuitry and the spatial localization of OT-innervating PCX neurons. Here we build upon standing literature to provide some answers to these questions through studies in mice of both sexes. First, we recorded the activity of OT neurons in awake mice while optically stimulating principal neurons in the aPCX and/or their association fibers in the OT while the mice were delivered odors. This uncovered evidence that PCX input indeed influences OT unit activity. We then used patch-clamp recordings and viral tracing to determine the connectivity of aPCX neurons upon OT neurons expressing dopamine receptor types D1 or D2, two prominent cell populations in the OT. These investigations uncovered that both populations of neurons receive monosynaptic inputs from aPCX glutamatergic neurons. Interestingly, this input originates largely from the ventrocaudal aPCX. These results shed light on some of the basic physiological properties of this pathway and the cell-types involved and provide a foundation for future studies to identify, among other things, whether this pathway has implications for perception.
SIGNIFICANCE STATEMENT Sensory cortices interact to process stimuli in manners considered essential for perception. Very little is known regarding interactions between olfactory cortices. The present study sheds light on some of the basic physiological properties of a particular intercortical pathway in the olfactory system and provides a foundation for future studies to identify, among other things, whether this pathway has implications for perception.
- Received June 18, 2019.
- Revision received October 8, 2019.
- Accepted October 11, 2019.
- Copyright © 2019 the authors
