Social hierarchy regulates ocular dominance plasticity in adult male mice

Abstract

We here show that social rank, as assessed by competition for a running wheel, influences ocular dominance plasticity in adult male mice. Dominant animals showed a clear ocular dominance shift after four days of MD, whereas their submissive cage mates did not. NMDA receptor activation, reduced GABA inhibition, and serotonin transmission were necessary for this plasticity, but not sufficient to explain the difference between dominant and submissive animals. In contrast, prefrontal dopamine concentration was higher in dominant than submissive mice, and systemic manipulation of dopamine transmission bidirectionally changed ocular dominance plasticity. Thus, we could show that a social hierarchical relationship influences ocular dominance plasticity in the visual cortex via higher-order cortices, most likely the medial prefrontal cortex. Further studies will be needed to elucidate the precise mechanisms by which this regulation takes place.

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Brain Structure and Function (2019) 224:3183–3199
https://doi.org/10.1007/s00429-019-01959-w
ORIGINAL ARTICLE
Social hierarchy regulates ocular dominance plasticity inadult male
mice
JennyBalog1· FranziskaHintz2· MarcelIsstas1· ManuelTeichert1· ChristineWinter2· KonradLehmann1,3
Received: 19 March 2019 / Accepted: 14 September 2019 / Published online: 25 September 2019
© Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
We here show that social rank, as assessed by competition for a running wheel, influences ocular dominance plasticity in
adult male mice. Dominant animals showed a clear ocular dominance shift after 4days of MD, whereas their submissive
cagemates did not. NMDA receptor activation, reduced GABA inhibition, and serotonin transmission were necessary for
this plasticity, but not sufficient to explain the difference between dominant and submissive animals. In contrast, prefrontal
dopamine concentration was higher in dominant than submissive mice, and systemic manipulation of dopamine transmission
bidirectionally changed ocular dominance plasticity. Thus, we could show that a social hierarchical relationship influences
ocular dominance plasticity in the visual cortex via higher-order cortices, most likely the medial prefrontal cortex. Further
studies will be needed to elucidate the precise mechanisms by which this regulation takes place.
Keywords Social dominance status· Ocular dominance plasticity· Primary visual cortex· Medial prefrontal cortex·
Optical imaging· Serotonin· GABA· NMDAR· Dopamine
Introduction
Dominance and submissiveness occur in all areas of life, not
only among people in school, work and other social situa-
tions, but in all group living animals (Stears etal. 2014). The
physiological background of this social condition is being
studied in many vertebrate (Morgan etal. 2002; Desjardins
and Fernald 2008; Kar etal. 2017; Jetz and Rubenstein
2011), and invertebrate species (Sbragaglia etal. 2017). A
social hierarchy entails a dominant–submissive relationship
between all individual pairs of animals within the group. As
a result, most animals will experience defeat and subordina-
tion frequently. In rodents, this experience has been shown
to induce stress (Blanchard etal. 1995), compromise mental
health (Prabhu etal. 2018), and impair learning (Goeckner
etal. 1973; Spritzer etal. 2004). More recent studies in pairs
of mice have confirmed that, indeed, learning ability deterio-
rates in submissive animals, which is not, however, directly
due to stress (Fitchett etal. 2005; Colas-Zelin etal. 2012;
Matzel etal. 2017).
Though an impact of social dominance or submissive-
ness on behavioural learning has thus been well established,
an effect on more basal cortical plasticity has not yet been
investigated. We have recently shown that paired, in contrast
to individual, housing of adult mice reinstated ocular domi-
nance plasticity (ODP, Balog etal. 2014), i.e., the propensity
of the primary visual cortex (V1) to shift its responsiveness
towards the open eye when one eye is experimentally closed.
While in female mice, which are not aggressive and do not
establish a clear hierarchy, this effect was seen irrespective
of the available space, it was only present in both male mice
of a pair if they disposed of a large arena. In a standard cage,
only one of the two would show plasticity.
The assumption was obvious that the difference in plastic-
ity was due to social dominance, the cramped space forcing
the males to arrange their relationship differently than in the
large arena. In this study, we tested this hypothesis and went
on to elucidate the mechanisms by which social status regu-
lates ODP in male mice. In addition to biochemical factors
acting within the visual cortex, we found dopamine, acting
* Konrad Lehmann
Konrad.Lehmann@uni-jena.de
1 Institut für Allgemeine Zoologie andTierphysiologie,
Friedrich Schiller-Universität Jena, Erbertstr. 1, 07743Jena,
Germany
2 Department ofPsychiatry andPsychotherapy, Charité
University Medicine Berlin, Berlin, Germany
3 GSI Helmholtzzentrum für Schwerionenforschung GmbH,
Abteilung Biophysik, Darmstadt, Germany
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