Distinct neural mechanisms mediate olfactory memory formation at different timescales.
Habituation is one of the oldest forms of learning, broadly expressed across sensory systems and taxa. Here, we demonstrate that olfactory habituation induced at different timescales (comprising different odor exposure and intertrial interval durations) is mediated by different neural mechanisms. First, the persistence of habituation memory is greater when mice are habituated on longer timescales. Second, the specificity of the memory (degree of cross-habituation to similar stimuli) also depends on induction timescale. Third, we demonstrate a pharmacological double dissociation between the glutamatergic mechanisms underlying short- and long-timescale odor habituation. LY341495, a class II/III metabotropic glutamate receptor antagonist, blocked habituation only when the induction timescale was short. Conversely, MK-801, an N-methyl-D-aspartate (NMDA) receptor antagonist, prevented habituation only when the timescale was long. Finally, whereas short-timescale odor habituation is mediated within the anterior piriform cortex, infusion of MK-801 into the olfactory bulbs prevented odor habituation only at longer timescales. Thus, we demonstrate two neural mechanisms underlying simple olfactory learning, distinguished by their persistence and specificity, mediated by different olfactory structures and pharmacological effectors, and differentially utilized based solely on the timescale of odor presentation.
McNamara
Ann Marie
AM
Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA.
Magidson
Phillip D
PD
Linster
Christiane
C
Wilson
Donald A
DA
Cleland
Thomas A
TA
D000596:Amino Acids / Q000494:pharmacology; D000818:Animals; D001931:Brain Mapping; D016291:Dizocilpine Maleate / Q000008:administration & dosage / Q000494:pharmacology; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D006185:Habituation, Psychophysiologic / Q000187:drug effects; D007267:Injections; D008297:Male; D008568:Memory / Q000502:physiology*; D051379:Mice; D008815:Mice, Inbred Strains; D009812:Odorants; D009830:Olfactory Bulb / Q000187:drug effects / Q000502:physiology; D009833:Olfactory Pathways / Q000187:drug effects / Q000502:physiology*; D012903:Smell; D013997:Time Factors; D014966:Xanthenes / Q000494:pharmacology
D000596:Amino Acids; D018691:Excitatory Amino Acid Antagonists; C114624:LY 341495; D014966:Xanthenes; D016291:Dizocilpine Maleate