How the brain encodes social rank and 'winning mindset'
In mice, one area of the brain is constantly tuned in to whether nearby animals are higher or lower in social hierarchy

Date:
March 16, 2022
Source:
Salk Institute
Summary:
Researchers have made inroads into understanding how the mammalian
brain encodes social rank and uses this information to shape
behaviors. In mice engaged in a competition, the team discovered,
patterns of brain activity differ depending on the social rank
of the opposing animal. Moreover, the scientists could use brain
readouts to accurately predict which animal would win a food reward
-- the victor was not always the more socially dominant animal,
but the one more engaged in a 'winning mindset.'


FULL STORY ==========================================================================
If you're reaching for the last piece of pizza at a party and see another
hand going for it at the same time, your next move probably depends
both on how you feel and whom the hand belongs to. Your little sister
-- you might go ahead and grab the pizza. Your boss -- you're probably
more likely to step back and give up the slice. But if you're hungry
and feeling particularly confident, you might go for it.


==========================================================================
Now, Salk researchers have made inroads into understanding how the
mammalian brain encodes social rank and uses this information to shape behaviors -- such as whether to fight for that last pizza slice. In mice engaged in a competition, the team discovered, patterns of brain activity differ depending on the social rank of the opposing animal. Moreover, the scientists could use brain readouts to accurately predict which animal
would win a food reward - - the victor was not always the more socially dominant animal, but the one more engaged in a "winning mindset." The
findings were published in Nature on March 16, 2022.

"Most social species organize themselves into hierarchies that guide
each individual's behavior," says senior author Kay Tye, professor
in Salk's Systems Neurobiology Laboratory and Howard Hughes Medical
Institute Investigator.

"Understanding how the brain mediates this may help us understand the
interplay between social rank, isolation, and psychiatric diseases, such
as depression, anxiety, or even substance abuse." Researchers already
knew that an area of the brain called the medial prefrontal cortex (mPFC)
was responsible for representing social rank in mammals; alterations to
a mouse's mPFC change an animal's dominance behavior. But it was unknown
how the mPFC represented this information and which neurons (if any)
were involved in altering dominance behavior.

In the new study, Tye and her team let groups of four mice share a cage, allowing a social hierarchy to naturally develop -- some animals became
more dominant and others more subordinate. Then, the researchers selected
pairs of cohabitating mice to compete for food rewards in a "round robin" tournament style structure.

To capture the brain activity of the animals, as well as slight,
difficult to measure differences in their behavior as they competed, the researchers spearheaded several new technologies. They used new wireless devices to record brain activity in free-roaming animals and developed a multi-animal artificial intelligence tracking tool to follow the movements
of the mice over time, even when two animals looked identical. Finally,
they turned to new modeling approaches to analyze the data.



==========================================================================
As soon as the mice were paired up, the scientists discovered, the
activity of neurons in their mPFC could predict -- with 90 percent
certainty -- the rank of their opponent.

"We expected that the animals might only signal rank when they
heard a beep to start the competition," says co-first author Nancy Padilla-Coreano, an assistant professor at the University of Florida,
who carried out the work while she was a postdoctoral fellow at Salk. "But
it turns out that animals are walking around with this representation of
social rank in their brain all the time." When the researchers next asked whether the activity of the mPFC neurons was associated with behavior,
they found something surprising. The brain activity patterns were linked
with slight changes in behavior, such as how fast a mouse moved, and they
also could predict -- a full 30 seconds before the competition started --
which mouse would win the food reward.

While the more dominant mouse was usually predicted to win, sometimes the
model accurately predicted that the subordinate animal would win. The
model, the team says, was capturing competitive success, or what some
people might call a "winning mindset." Just as you might sometimes be
in a more competitive mood and be more likely to snatch that pizza slice
before your boss, a subordinate mouse might be in a more "winning mindset"
than a more dominant animal and end up winning.



==========================================================================
The areas of the mPFC associated with social rank and competitive
success are adjacent to one another, the researchers discovered, and
highly connected.

Signals on social rank, they say, impact the state of the brain involved
in competitive success. In other words, a subordinate animal's confidence
and "winning mindset" may partially diminish when faced with the alpha
mouse.

"This is the first time we've been able to capture these internal
states that connect social rank to behavior," says Kanha Batra, a
graduate student in the Tye lab and co-first author of the paper. "At
any timepoint, we could predict an animal's next move from brain activity
using these internal states." The researchers also showed that changes
in brain activity occurred when the animals were in competition versus
when they were collecting rewards alone.

However, social rank of the animals' living group could still be decoded
from the brain activity even when animals were alone.

"This is all further evidence to suggest that we are in different brain
states when we are with others compared to when we're alone," says Tye,
holder of the Wylie Vale Chair. "Regardless of who you're with, if
you're aware of other people around you, your brain is using different neurons." Next, the scientists will examine how and when the animals' representations of social rank first develop in the brain, as well as
how other types of behaviors are affected.

Other authors included Makenzie Patarino, Sebastien B. Hausmann, Reesha
Patel, Srishti Mishra, Deryn O. LeDuke, Jasmin Revanna, Hao Li, Matilde
Borio, Rachelle Pamintuan, Aneesh Bal, Laurel R. Keyes, Avraham Libster,
Romy Wichmann, Fergil Mills, Felix H. Taschbach and Gillian A. Matthews
of Salk; Zexin Chen, Hao-Shu Fang and Cewu Lu of Shanghai Jiao Tong
University; Rachel R. Rock, Ruihan Zhang, Javier C. Weddington and
Ila R. Fiete of Massachusetts Institute of Technology; Yu Eva Zhang of University of California San Diego; and James P. Curley of University
of Texas at Austin.

The work was supported by the Howard Hughes Medical Institute, National Institutes of Health (R01-MH115920, Pioneer Award DP1-AT009925 and K99 MH124435-01), JPB Foundation, Dolby Family Fund, the Kavli Foundation,
the Simons Center for the Social Brain, Ford Foundation, L'Oreal For
Women In Science, Burroughs Wellcome Fund, AI Institute, SJTU, Shanghai
Qi Zhi Institute, and Meta Technology Group.


========================================================================== Story Source: Materials provided by Salk_Institute. Note: Content may
be edited for style and length.


========================================================================== Journal Reference:
1. Nancy Padilla-Coreano, Kanha Batra, Makenzie Patarino, Zexin
Chen, Rachel
R. Rock, Ruihan Zhang, Se'bastien B. Hausmann, Javier C. Weddington,
Reesha Patel, Yu E. Zhang, Hao-Shu Fang, Srishti Mishra, Deryn
O. LeDuke, Jasmin Revanna, Hao Li, Matilde Borio, Rachelle
Pamintuan, Aneesh Bal, Laurel R. Keyes, Avraham Libster, Romy
Wichmann, Fergil Mills, Felix H.

Taschbach, Gillian A. Matthews, James P. Curley, Ila R. Fiete,
Cewu Lu, Kay M. Tye. Cortical ensembles orchestrate social
competition through hypothalamic outputs. Nature, 2022; DOI:
10.1038/s41586-022-04507-5 ==========================================================================

Link to news story: https://www.sciencedaily.com/releases/2022/03/220316120832.htm

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