GABAb receptors tune cortical feedback to the olfactory bulb
Journal of Neuroscience. 2016-08-10; 36(32): 8289-8304
DOI: 10.1523/JNEUROSCI.3823-15.2016
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Mazo C(1), Lepousez G(1), Nissant A(1), Valley MT(1), Lledo PM(2).
Author information:
(1)Laboratory for Perception and Memory, Institut Pasteur, F-75015 Paris,
France, and Centre National de la Recherche Scientifique, Unité Mixte de
Recherche 3571, F-75015 Paris, France.
(2)Laboratory for Perception and Memory, Institut Pasteur, F-75015 Paris,
France, and Centre National de la Recherche Scientifique, Unité Mixte de
Recherche 3571, F-75015 Paris, France .
Sensory perception emerges from the confluence of sensory inputs that encode the
composition of external environment and top-down feedback that conveys
information from higher brain centers. In olfaction, sensory input activity is
initially processed in the olfactory bulb (OB), serving as the first central
relay before being transferred to the olfactory cortex. In addition, the OB
receives dense connectivity from feedback projections, so the OB has the
capacity to implement a wide array of sensory neuronal computation. However,
little is known about the impact and the regulation of this cortical feedback.
Here, we describe a novel mechanism to gate glutamatergic feedback selectively
from the anterior olfactory cortex (AOC) to the OB. Combining in vitro and in
vivo electrophysiological recordings, optogenetics, and fiber-photometry-based
calcium imaging applied to wild-type and conditional transgenic mice, we explore
the functional consequences of circuit-specific GABA type-B receptor (GABABR)
manipulation. We found that activation of presynaptic GABABRs specifically
depresses synaptic transmission from the AOC to OB inhibitory interneurons, but
spares direct excitation to principal neurons. As a consequence, feedforward
inhibition of spontaneous and odor-evoked activity of principal neurons is
diminished. We also show that tunable cortico-bulbar feedback is critical for
generating beta, but not gamma, OB oscillations. Together, these results show
that GABABRs on cortico-bulbar afferents gate excitatory transmission in a
target-specific manner and thus shape how the OB integrates sensory inputs and
top-down information.
SIGNIFICANCE STATEMENT: The olfactory bulb (OB) receives top-down inputs from
the olfactory cortex that produce direct excitation and feedforward inhibition
onto mitral and tufted cells, the principal neurons. The functional role of this
feedback and the mechanisms regulating the balance of feedback excitation and
inhibition remain unknown. We found that GABAB receptors are expressed in
cortico-bulbar axons that synapse on granule cells and receptor activation
reduces the feedforward inhibition of spontaneous and odor-driven mitral and
tufted cells’ firing activity. In contrast, direct excitatory inputs to these
principal neurons remain unchanged. This study demonstrates that activation of
GABAB receptors biases the excitation/inhibition balance provided by cortical
inputs to the OB, leading to profound effects on early stages of sensory
information processing.
Copyright © 2016 the authors 0270-6474/16/368289-16$15.00/0.