Dopaminergic mechanisms of dynamical social specialization | Nature

## Summary
Over time, the number of lever presses (#LP) increased and the number of nose pokes decreased, indicating that mice had learned the association between lever press and food retrieval (Fig. 1c , left, and Extended Data Fig. 1a ). Additionally, we found a correlation between VTA dopaminergic activity at lever press and the time taken to reach the food magazine (Extended Data Fig. 1c , bottom). Finally, spontaneous VTA dopaminergic neuron activity, recorded post-experiment in anaesthetized males, showed higher firing frequency in Achievers than in Storers (Fig. 1k and Extended Data Fig. 1g ), suggesting a link between VTA dopaminergic activity and foraging strategies 32 , 37 , 38 . Male and female mice performed a similar number of lever presses, but females achieved significantly fewer complete sequences (Fig. 2c and Extended Data Fig. 2a ), reflecting higher latencies between lever press and food retrieval, and more consecutive lever presses before consumption (Extended Data Fig. 2b ).

## Article Content
Download PDF
Subjects
Dynamical systems
Learning algorithms
Neural circuits
Reward
Social behaviour
Abstract
Social organization and division of labour are fundamental to animal societies
1
,
2
,
3
, yet how these structures emerge from individual interactions and are shaped by neuromodulation remains unclear. Here, using behavioural tracking in a semi-natural environment, neural recordings and computational models that integrate reinforcement learning and social condition, we show that triads of isogenic mice develop specialized roles spontaneously while solving a foraging task under social constraints. Notably, despite minor intra-sex differences in behaviour when mice were tested alone, male triads formed stable worker–scrounger relationships driven by competition, whereas female triads adopted uniform, cooperative strategies. These sex-divergent roles were shaped by dopaminergic activity in the ventral tegmental area. Model analysis revealed how intra-sex and inter-sex parameter differences in resource exploitation, combined with contingent social interactions, drive behavioural specialization and division of labour. Most notably, it highlighted how contingency, amplified by competition, magnifies individual differences and shapes social profiles. The plastic, adaptive nature of social organization was apparent when sex mixing or reintroducing experienced individuals into naive groups reshaped role distribution. Furthermore, dopaminergic manipulations confirmed this plasticity, reshaping roles and altering group structure. Our findings support a multi-scale feedback loop whereby social context shapes neural states, which in turn reinforce behavioural specialization and stabilize social structures.
Main
Social animals interact and coordinate their behaviours to form social organizations—structured patterns of relationships and interactions that stabilize into collective forms (for example, division of labour and norms) and specialized roles
3
,
4
,
5
,
6
,
7
. A key challenge in behavioural science is deciphering how individual differences in behaviour emerge, how they contribute to collective actions and how they are linked to neural activity. While the broad effects of social organization on individual behaviour and specialization are well documented
8
,
9
,
10
,
11
,
12
, the underlying cognitive and neurophysiological mechanisms remain largely unexplored, mainly because of the difficulty of studying such mechanisms in controlled, artificial social settings that also allow neurobiological investigation.
In social groups, the production of and access to shared resources drive strategies such as competition or cooperation
2
,
8
,
13
. The producer–scrounger game illustrates this dynamic: some individuals produce resources, others exploit them
1
,
2
,
14
,
15
. Thus, foraging strategies span from independent food acquisition to exploiting others’ efforts, balancing effort, risk and reward under ecological and social constraints
13
. Evolutionary game theory
16
predicts stable equilibria between such strategies, but typically assumes that behaviours are predetermined and stable
17
, overlooking the internal mechanisms that guide an individual’s behaviour, including the neural and cognitive processes that grant adaptative, learning-based flexible strategies
17
,
18
,
19
. Central to this adaptability is dopaminergic signalling, which reinforces rewarded actions by signalling when reward is larger than expected
20
,
21
,
22
,
23
, including social reward
24
,
25
. A second key process is the exploration–exploitation trade-off
26
,
27
,
28
,
29
, whereby individuals must choose between exploiting known options and exploring alternatives, a process in which dopamine has also been implicated
30
,
31
,
32
,
33
,
34
,
35
.
Here we hypothesize that social foraging strategies, including producer–scrounger dynamics, emerge flexibly through socially constrained reinforcement learning. In particular, we suggest that dopaminergic signalling shapes variability in learning and decision policies, thereby contributing to behavioural specialization. As social organizations forms, individuals adjust actions on the basis of expected payoffs, which in turn modify neural activity and learning rules, ultimately stabilizing social roles. Recent advances in continuous animal tracking and behaviour quantification in semi-naturalistic settings
36
,
37
,
38
,
39
,
40
enable detailed measurements of how individuals interact and adapt their strategies over time. Using these approaches, we examined how foraging specialization emerges in small groups (
n
= 3) of isogenic mice housed in a controlled semi-natural environment.
Two foraging strategies in lone mice
We first assessed mice foraging behaviour and underlying neural mechanisms in a lone context. Female or male mice (
n
= 62) were placed alone in a 50 cm × 50 cm multi-compartment environment and tracked continuously for 5 days and 4 nights using the Live Mouse Tracker system
36
.

---

## Expert Analysis

### Merits
N/A

### Areas for Consideration
- Download PDF Subjects Dynamical systems Learning algorithms Neural circuits Reward Social behaviour Abstract Social organization and division of labour are fundamental to animal societies 1 , 2 , 3 , yet how these structures emerge from individual interactions and are shaped by neuromodulation remains unclear.
- A key challenge in behavioural science is deciphering how individual differences in behaviour emerge, how they contribute to collective actions and how they are linked to neural activity.
- Thus, foraging strategies span from independent food acquisition to exploiting others’ efforts, balancing effort, risk and reward under ecological and social constraints 13 .

### Implications
N/A

### Expert Commentary
This article covers fig, lever, social topics. Areas of concern are also raised. Readability: Flesch-Kincaid grade 0.0. Word count: 2316.