Two-photon imaging of D1 and D2 type neurons in the olfactory tubercle of behaving mice

Positive and negative associations acquired through olfactory experience
are thought to be especially strong and long-lasting. The conserved direct
olfactory sensory input to the ventral striatal olfactory tubercle (OT)
and its convergence with dense dopaminergic input to the OT could underlie
this privileged form of associative memory, but how this process occurs is
not well understood. We imaged the activity of the two canonical types of
striatal neurons, expressing D1 or D2 type dopamine receptors, in the OT
at cellular resolution while mice learned odor-outcome associations
ranging from aversive to rewarding. D1 and D2 neurons both responded to
rewarding and aversive odors. D1 neurons in the OT robustly and
bidirectionally represented odor valence, responding similarly to odors
predicting similar outcomes regardless of odor identity. This valence
representation persisted even in the absence of an instrumental response
to the odors and in the absence of the outcomes, indicating a true
transformation of odor sensory information by D1 OT neurons. In contrast,
D2 neuronal representation of the odor-outcome associations was weaker,
contingent on an instrumental response by the mouse, and D2 neurons were
more selective for odor identity than valence. Stimulus valence coding in
the OT was not modality invariant, with separate sets of D1 neurons
responding to odors and sounds predicting the same outcomes, suggesting
that integration of multimodal valence information happens downstream of
the OT. Our results point to distinct representation of identity and
valence of odor stimuli by D1 and D2 neurons in the OT.