Sex differences in neural and behavioral signatures of cooperation revealed by fNIRS hyperscanning

Abstract

Researchers from multiple fields have sought to understand how sex moderates human social behavior. While over 50 years of research has revealed differences in cooperation behavior of males and females, the underlying neural correlates of these sex differences have not been explained. A missing and fundamental element of this puzzle is an understanding of how the sex composition of an interacting dyad influences the brain and behavior during cooperation. Using fNIRS-based hyperscanning in 111 same- and mixed-sex dyads, we identified significant behavioral and neural sex-related differences in association with a computer-based cooperation task. Dyads containing at least one male demonstrated significantly higher behavioral performance than female/female dyads. Individual males and females showed significant activation in the right frontopolar and right inferior prefrontal cortices, although this activation was greater in females compared to males. Female/female dyad's exhibited significant inter-brain coherence within the right temporal cortex, while significant coherence in male/male dyads occurred in the right inferior prefrontal cortex. Significant coherence was not observed in mixed-sex dyads. Finally, for same-sex dyads only, task-related inter-brain coherence was positively correlated with cooperation task performance. Our results highlight multiple important and previously undetected influences of sex on concurrent neural and behavioral signatures of cooperation.

Figure 1. Participant arrangement and cooperation task structure.

(A) Participants were sat on opposite sides of a square table, in front of individual monitors and keyboards. (B) Trial stimulus sequence. Both participants were seated in front of their own computer screen and keyboard. Each trial began with a hollow gray circle appearing in the center of the screen for an unpredictable duration between 0.6 and 1.5 seconds. An abrupt change in the color of the circle from black to green initiated the participant’s response. Following both responses, a “win” or “lose” message was presented, depending on whether the inter-response latency of both participants was less than , where R1 and R2 are the response times for both participants respectively. A ‘+’ and ‘−’ sign was also presented, which indicated the faster/slower responder for each trial. The symbol on both participants’ left hand side of the screen corresponded to their response speed relative the their partner. Two 40 trial cooperation task blocks were separated by a 30 second rest period. Task-related inter-brain coherence was calculated as the average coherence during both task blocks minus coherence during rest .

Figure 2. fNIRS regions of interest.

(A) The medial optode column of a 3 × 3 fNIRS optode patch was placed over the midsagital line and directly above the brow. Four three-channel regions (colored triangles) were identified a priori. The anterior edge of a 2 × 3 fNIRS optode patch as placed over the interauricular arc and directly above the T4 10/20 location. (B) A single region of interest (blue rectangle) was established in the temporal region.

Figure 3. Cooperation performance across dyads.

Analysis of variance identified significant performance differences across groups (p = 0.002). Specifically, male/male (p = 0.003) and male/female (p = 0.004) significantly outperformed female/female groups. The bold mid-line within each box and whisker plot provides the median performance for each group. Each box represents the cooperation task performance distribution for 50% of the dyads within each sex pairing. The whiskers extending from each colored box represent the minimum and maximum performance, and the dots represent outlying performance. Outliers were defined as any value less than or equal to 1.5 times the group inter-quartile range.

Figure 4. Cortical activation during cooperation.

(A) Investigation of cortical activation across each region of interest identified significant increases in activation relative to rest within the right frontopolar (p = 0.027) and right inferior (p < 0.001) regions. Pairwise comparisons revealed significant activation differences between the right inferior and right temporal (p < 0.001). (B) Female participants elicited significantly greater cortical activation compared to males (p = 0.013).

Figure 5. Inter-brain coherence increase within the right inferior and right temporal cortices.

A significant increase in inter-brain coherence was identified in male/male groups’ right inferior pre-frontal cortex (p = 0.020), and was significantly greater than male/female (p = 0.003) and female/female (p = 0.046) groups. Moreover, a significant increase in inter-brain coherence was identified in female/female groups right temporal cortex (p = 0.005). Female/female coherence in this region was significantly greater than male/female group coherence (p = 0.039).

Figure 6. Relationship between cooperation performance and task-related inter-brain coherence.

(A) Cooperation performance significantly predicts inter-brain coherence (r = 0.603, p = 0.024) across all regions. (B) The relationship between cooperation performance and inter-brain coherence was significant for male/male (r = 0.862, p = 0.035) and female/female (r = 1.195, p = 0.012) groups. This relationship was positive within these groups, indicating that greater behavioral performance coincided with enhanced inter-brain coherence. Conversely, this relationship within male/female pairs was non-significant (p = 0.537, r = −0.147).