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Experience-Dependent Plasticity in Accessory Olfactory Bulb Interneurons following Male-Male Social Interaction.

The Journal of neuroscience : the official journal of the Society for Neuroscience | 2017

Chemosensory information processing in the mouse accessory olfactory system guides the expression of social behavior. After salient chemosensory encounters, the accessory olfactory bulb (AOB) experiences changes in the balance of excitation and inhibition at reciprocal synapses between mitral cells (MCs) and local interneurons. The mechanisms underlying these changes remain controversial. Moreover, it remains unclear whether MC-interneuron plasticity is unique to specific behaviors, such as mating, or whether it is a more general feature of the AOB circuit. Here, we describe targeted electrophysiological studies of AOB inhibitory internal granule cells (IGCs), many of which upregulate the immediate-early gene Arc after male-male social experience. Following the resident-intruder paradigm, Arc-expressing IGCs in acute AOB slices from resident males displayed stronger excitation than nonexpressing neighbors when sensory inputs were stimulated. The increased excitability of Arc-expressing IGCs was not correlated with changes in the strength or number of excitatory synapses with MCs but was instead associated with increased intrinsic excitability and decreased HCN channel-mediated IH currents. Consistent with increased inhibition by IGCs, MCs responded to sensory input stimulation with decreased depolarization and spiking following resident-intruder encounters. These results reveal that nonmating behaviors drive AOB inhibitory plasticity and indicate that increased MC inhibition involves intrinsic excitability changes in Arc-expressing interneurons.SIGNIFICANCE STATEMENT The accessory olfactory bulb (AOB) is a site of experience-dependent plasticity between excitatory mitral cells (MCs) and inhibitory internal granule cells (IGCs), but the physiological mechanisms and behavioral conditions driving this plasticity remain unclear. Here, we report studies of AOB neuronal plasticity following male-male social chemosensory encounters. We show that the plasticity-associated immediate-early gene Arc is selectively expressed in IGCs from resident males following the resident-intruder assay. After behavior, Arc-expressing IGCs are more strongly excited by sensory input stimulation and MC activation is suppressed. Arc-expressing IGCs do not show increased excitatory synaptic drive but instead show increased intrinsic excitability. These data indicate that MC-IGC plasticity is induced after male-male social chemosensory encounters, resulting in enhanced MC suppression by Arc-expressing IGCs.

Pubmed ID: 28659282 RIS Download

Associated grants

  • Agency: NIDCD NIH HHS, United States
    Id: R00 DC011780
  • Agency: NIDCD NIH HHS, United States
    Id: R01 DC015784
  • Agency: NIDA NIH HHS, United States
    Id: T32 DA007290

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This is a list of tools and resources that we have found mentioned in this publication.


Anti-GFP antibody (antibody)

RRID:AB_300798

This polyclonal targets GFP

View all literature mentions

Anti-Arc (antibody)

RRID:AB_887694

This polyclonal targets Arc

View all literature mentions

pClamp (software resource)

RRID:SCR_011323

Software suite for electrophysiology data acquisition and analysis by Molecular Devices. Used for the control and recording of voltage clamp, current clamp, and patch clamp experiments. The software suite consists of Clampex 11 Software for data acquisition, AxoScope 11 Software for background recording, Clampfit 11 Software for data analysis, and optional Clampfit Advanced Analysis Module for sophisticated and streamlined analysis.

View all literature mentions

ImageJ (software resource)

RRID:SCR_003070

Open source Java based image processing software program designed for scientific multidimensional images. ImageJ has been transformed to ImageJ2 application to improve data engine to be sufficient to analyze modern datasets.

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B6;129S6-Gt(ROSA)26Sortm9(CAG-tdTomato)Hze/J (organism)

RRID:IMSR_JAX:007905

Mus musculus with name B6;129S6-Gt(ROSA)26Sortm9(CAG-tdTomato)Hze/J from IMSR.

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B6;129S1-Trpc2tm1Dlc/J (organism)

RRID:IMSR_JAX:021208

Mus musculus with name B6;129S1-Trpc2tm1Dlc/J from IMSR.

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C57BL/6-Arctm1Stl/J (organism)

RRID:IMSR_JAX:007662

Mus musculus with name C57BL/6-Arctm1Stl/J from IMSR.

View all literature mentions

pClamp (software resource)

RRID:SCR_011323

Software suite for electrophysiology data acquisition and analysis by Molecular Devices. Used for the control and recording of voltage clamp, current clamp, and patch clamp experiments. The software suite consists of Clampex 11 Software for data acquisition, AxoScope 11 Software for background recording, Clampfit 11 Software for data analysis, and optional Clampfit Advanced Analysis Module for sophisticated and streamlined analysis.

View all literature mentions

Anti-GFP antibody (antibody)

RRID:AB_300798

This polyclonal targets GFP

View all literature mentions

Anti-Arc (antibody)

RRID:AB_887694

This polyclonal targets Arc

View all literature mentions

ImageJ (software resource)

RRID:SCR_003070

Open source Java based image processing software program designed for scientific multidimensional images. ImageJ has been transformed to ImageJ2 application to improve data engine to be sufficient to analyze modern datasets.

View all literature mentions

B6;129S6-Gt(ROSA)26Sortm9(CAG-tdTomato)Hze/J (organism)

RRID:IMSR_JAX:007905

Mus musculus with name B6;129S6-Gt(ROSA)26Sortm9(CAG-tdTomato)Hze/J from IMSR.

View all literature mentions

B6;129S1-Trpc2tm1Dlc/J (organism)

RRID:IMSR_JAX:021208

Mus musculus with name B6;129S1-Trpc2tm1Dlc/J from IMSR.

View all literature mentions

C57BL/6-Arctm1Stl/J (organism)

RRID:IMSR_JAX:007662

Mus musculus with name C57BL/6-Arctm1Stl/J from IMSR.

View all literature mentions