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Functional properties of cortical feedback projections to the olfactory bulb.

ABSTRACT: Sensory perception is not a simple feed-forward process, and higher brain areas can actively modulate information processing in "lower" areas. We used optogenetic methods to examine how cortical feedback projections affect circuits in the first olfactory processing stage, the olfactory bulb. Selective activation of back projections from the anterior olfactory nucleus/cortex (AON) revealed functional glutamatergic synaptic connections on several types of bulbar interneurons. Unexpectedly, AON axons also directly depolarized mitral cells (MCs), enough to elicit spikes reliably in a time window of a few milliseconds. MCs received strong disynaptic inhibition, a third of which arises in the glomerular layer. Activating feedback axons in vivo suppressed spontaneous as well as odor-evoked activity of MCs, sometimes preceded by a temporally precise increase in firing probability. Our study indicates that cortical feedback can shape the activity of bulbar output neurons by enabling precisely timed spikes and enforcing broad inhibition to suppress background activity.

SUBMITTER: Markopoulos F

PROVIDER: S-EPMC3530161 | biostudies-other | 2012 Dec

REPOSITORIES: biostudies-other

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Functional properties of cortical feedback projections to the olfactory bulb.

Markopoulos Foivos F Rokni Dan D Gire David H DH Murthy Venkatesh N VN

Neuron 20121201 6

Sensory perception is not a simple feed-forward process, and higher brain areas can actively modulate information processing in "lower" areas. We used optogenetic methods to examine how cortical feedback projections affect circuits in the first olfactory processing stage, the olfactory bulb. Selective activation of back projections from the anterior olfactory nucleus/cortex (AON) revealed functional glutamatergic synaptic connections on several types of bulbar interneurons. Unexpectedly, AON axo ...[more]

PMID: 23259952

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Project description:The mammalian olfactory bulb (OB) has a vast population of dopamine (DA) neurons, whose function is to increase odor discrimination through mostly inhibitory synaptic mechanisms. However, it is not well understood whether there is more than one neuronal type of OB DA neuron, how these neurons respond to different stimuli, and the ionic mechanisms behind those responses. In this study, we used a transgenic rat line (hTH-GFP) to identify fluorescent OB DA neurons for recording via whole-cell electrophysiology. These neurons were grouped based on their localization in the glomerular layer ("Top" vs. "Bottom") with these largest and smallest neurons grouped by neuronal area ("Large" vs. "Small," in μm2). We found that some membrane properties could be distinguished based on a neuron's area, but not by its glomerular localization. All OB DA neurons produced a single action potential when receiving a sufficiently depolarizing stimulus, while some could also spike multiple times when receiving weaker stimuli, an activity that was more likely in Large than Small neurons. This single spiking activity is likely driven by the Na+ current, which showed a sensitivity to inactivation by depolarization and a relatively long time constant for the removal of inactivation. These recordings showed that Small neurons were more sensitive to inactivation of Na+ current at membrane potentials of -70 and -60 mV than Large neurons. The hyperpolarization-activated H-current (identified by voltage sags) was more pronounced in Small than Large DA neurons across hyperpolarized membrane potentials. Lastly, to mimic a more physiological stimulus, these neurons received ramp stimuli of various durations and current amplitudes. When stimulated with weaker/shallow ramps, the neurons needed less current to begin and end firing and they produced more action potentials at a slower frequency. These spiking properties were further analyzed between the four groups of neurons, and these analyses support the difference in spiking induced with current step stimuli. Thus, there may be more than one type of OB DA neuron, and these neurons' activities may support a possible role of being high-pass filters in the OB by allowing the transmission of stronger odor signals while inhibiting weaker ones.

Dataset Information

Functional properties of cortical feedback projections to the olfactory bulb.

Publications

Functional properties of cortical feedback projections to the olfactory bulb.

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