Parvalbumin-Expressing Interneurons Linearly Control Olfactory Bulb Output

Abstract

SUMMARY In the olfactory bulb, odor representations by principal mitral cells are modulated by local inhibitory circuits. While dendrodendritic synapses between mitral and granule cells are typically thought to be a major source of this modulation, the contributions of other inhibitory neurons remain unclear. Here we demonstrate the functional properties of olfactory bulb parvalbumin-expressing interneurons (PV cells) and identify their important role in odor coding. Using paired recordings, we find that PV cells form reciprocal connections with the majority of nearby mitral cells, in contrast to the sparse connectivity between mitral and granule cells. In vivo calcium imaging in awake mice reveals that PV cells are broadly tuned to odors. Furthermore, selective PV cell inactivation enhances mitral cell responses in a linear fashion while maintaining mitral cell odor preferences. Thus, dense connections between mitral and PV cells underlie an inhibitory circuit poised to modulate the gain of olfactory bulb output.

Modulation of olfactory bulb network activity by serotonin: synchronous inhibition of mitral cells mediated by spatially localized GABAergic microcircuits

“…A wide variety of morphologically defined interneuron subtypes has been identified in the EPL and GCL that could potentially form axonal connections with MCs (Schneider and Macrides 1978;Pressler and Strowbridge 2006;Kosaka and Kosaka 2011;Pressler et al 2013). Recent studies (Kato et al 2013;Miyamichi et al 2013) described a new class of parvalbumin (PV)-immunoreactive interneuron located in the external plexiform layer that could potentially mediate the synchronous IPSCs we observe in MCs in 5-HT. Alternatively, one or more subtypes of large "short-axon" interneurons in GCL, such as Blanes cells (Pressler and Strowbridge 2006) and Golgi cells (Pressler et al 2013), may contact MCs in addition to GCs.…”

Role of intraglomerular circuits in shaping temporally structured responses to naturalistic inhalation-driven sensory input to the olfactory bulb

“…At the circuit level, the network model could also be expanded to include an emerging diversity of inhibitory circuits in the glomerular and infraglomerular layers, such as FFI mediated by short-axon cells (Liu et al 2013;Whitesell et al 2013), PG cell-mediated FFI of ET cells (Gire and Schoppa 2009;Shao et al 2012), GABAergic input to MCs from recently described parvalbumin-expressing external plexiform interneurons (Huang et al 2013;Kato et al 2013;Miyamichi et al 2013) and RI between PG and MCs (Murphy et al 2005). Each of these circuits has the potential to contribute further to inhalation-linked temporal patterning.…”

Construction of functional neuronal circuitry in the olfactory bulb

“…Propagated spikes in granule cells also mediate lateral inhibition to other mitral/tufted cells [63]. However, connectivity between mitral/tufted cells and granule cells are very sparse [25,64]. Indeed, a sparse, rather than dense, receptive field better explains odor response profiles of mitral/tufted cells in vivo [65,66].…”

“…Lateral dendrites of mitral/tufted cells form dense connections with yet another interneurons: parvalbumin-expressing interneurons (PV neurons) located in the external plexiform layer [64,67,68]. PV neurons form dense connections with mitral/tufted cells.…”