Glutamatergic Neurons in the Piriform Cortex Influence the Activity of D1- and D2-Type Receptor-Expressing Olfactory Tubercle Neurons

J Neurosci. 2019 Nov 27;39(48):9546-9559. doi: 10.1523/JNEUROSCI.1444-19.2019. Epub 2019 Oct 18.

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.

Keywords: connectivity; olfaction; olfactory cortex; ventral striatum.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Glutamic Acid / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Odorants
  • Olfactory Receptor Neurons / drug effects
  • Olfactory Receptor Neurons / metabolism*
  • Olfactory Tubercle / drug effects
  • Olfactory Tubercle / metabolism*
  • Piriform Cortex / drug effects
  • Piriform Cortex / metabolism*
  • Receptors, Dopamine D1 / biosynthesis*
  • Receptors, Dopamine D1 / genetics
  • Receptors, Dopamine D2 / biosynthesis*
  • Receptors, Dopamine D2 / genetics
  • Smell / physiology

Substances

  • DRD2 protein, mouse
  • Drd1 protein, mouse
  • Receptors, Dopamine D1
  • Receptors, Dopamine D2
  • Glutamic Acid