Interbrain cortical synchronization encodes multiple aspects of social interactions in monkey pairs

Abstract

While it is well known that the primate brain evolved to cope with complex social contingencies, the neurophysiological manifestation of social interactions in primates is not well understood. Here, concurrent wireless neuronal ensemble recordings from pairs of monkeys were conducted to measure interbrain cortical synchronization (ICS) during a whole-body navigation task that involved continuous social interaction of two monkeys. One monkey, the passenger, was carried in a robotic wheelchair to a food dispenser, while a second monkey, the observer, remained stationary, watching the passenger. The two monkeys alternated the passenger and the observer roles. Concurrent neuronal ensemble recordings from the monkeys' motor cortex and the premotor dorsal area revealed episodic occurrence of ICS with probability that depended on the wheelchair kinematics, the passenger-observer distance, and the passenger-food distance - the social-interaction factors previously described in behavioral studies. These results suggest that ICS represents specific aspects of primate social interactions.

Figure 1

Interbrain cortical synchronization (ICS) during the navigation task. (A) Locations of cortical implants in three monkeys (C,J, and K). Neuronal-ensemble recordings were conducted in M1 (red dots) and PMd (blue dots), in both hemispheres. (B) The experimental setup. Two monkeys (passenger and observer) were placed in a 5.0-by-3.9 m room. The passenger sat in an electrically actuated wheelchair. The observer sat in a stationary chair placed in the corner of the room. During each trial, the passenger moved from a starting location (shown on the left) to a stationary grape dispenser. Five representative routes of the wheelchair are plotted in different colors. These routes were randomly generated by a computer program. (C) Color plots of neuronal-ensemble activity for two representative trials. Each horizontal line corresponds to a unit. Color represents normalized (z-scored) firing rate of 69 units were recorded in monkey C (observer in this experiment) and 47 in monkey K (passenger). Episodes of ICS are marked by red horizontal lines. (D) Continuous evaluation of ICS for the trials shown in (C). Instantaneous values of the distance correlation were computed with a sliding window, of the same 3-s width as the red bars in (C). Correlation peaks are marked by arrows. (E) Wheelchair routes for the same trials as in (C) and (D). The routes are color-coded to indicate ICS.

Figure 2

The dependence of ICS on wheelchair position and velocity, expressed as conditional probability of ICS episodes. (A–D) Probability of ICS episodes as a function of room x,y coordinates. The values of probability at each pixel are averaged with immediate neighbors and are color coded. The one-dimensional bars below each two-dimensional plot show the dependence of probability on the distance between the passenger and food reward (top), and between the passenger and the observer (bottom). The results for monkey pair C-K are shown in (A,C) and for monkey pair C–J in (B,D). Monkey C was either passenger (panels on the left) or observer (panels on the right). In (A,B) the observer was in the right corner of the room (relative to the passenger at the starting location), and the grape dispenser was in the left corner. In (C,D), the locations of the observer and grape dispenser were swapped. (E,F) Color-coded probability of ICS episodes as a function of wheelchair velocity for monkey pairs C–K (E) and C–J (F). Horizontal axis corresponds to rotational velocity, and vertical axis corresponds to translational velocity. (See Fig. S4 for the number of samples contributed to each pixel).

Figure 3

Modulation of passenger’s and observer’s units to wheelchair kinematics. (A) Modulation patterns to rotational (horizontal axis) and translational (vertical axis) velocity in a representative PMd unit recorded in monkey C. Color represents normalized (z-scored) firing rate. In these experiments, monkey C was paired with monkey K, and acted as passenger (left panels) or observer (right panels). ICS episodes were detected, and neuronal modulation was assessed separately when these episodes were present (ICS+, top panels) and absent (ICS−, bottom panels). (B) Modulation patterns in an M1 unit recorded in monkey J. Monkey J was paired with monkey C. Conventions as in (B). (C) Bar plots representing average proportion of units modulated to the wheelchair velocity (left panel) and acceleration (right panel) for different monkey pairs, monkeys, and monkey roles (passenger or observer). Values are shown separately for the presence and absence of ICS episodes. Error bars represent 95% confidence interval obtained by 1,000 bootstrap replicates. (D) Averaged neural modulation depth to the wheelchair velocity (left panel) and acceleration (right panel). Conventions as in (C).

Figure 4

Modulation of passenger’s and observer’s units to the wheelchair room coordinates. (A) Modulation of a PMd unit recorded in monkey C. Color represents normalized (z-scored) firing rate. In these experiments, monkey C was paired with monkey K, and acted as passenger (left panels) or observer (right panels). The observer was seated in the left corner (left panels) or right corner (right panels) (relative to the passenger at the starting location). Neuronal modulation was assessed separately when ICS episodes were present (ICS+, top panels) or absent (ICS−, bottom panels). (B) Modulation of a PMd unit recorded in monkey K. Monkey K was paired with monkey C. Conventions as in (A). (C) Bar plots representing average proportion of units modulated to wheelchair position for different monkey pairs, monkeys, and monkey roles (passenger or observer). Proportions are shown separately for the presence and absence of ICS episodes. Error bars represent 95% confidence interval obtained by 1,000 bootstrap replicates. (D) Averaged modulation depth. Conventions as in (C).

Figure 5

Neuronal activity patterns across monkeys and ICS conditions. (A) Bar plots represent average modulation depth to the distance between the passenger and observer. Results are presented separately for different monkey pairs, monkeys, monkey roles (passenger or observer), and the presence/absence of ICS episodes. Error bars represent 95% confidence interval obtained by 1,000 bootstrap replicates. Panels (B–E) use the same conventions as in (A). (B) Average modulation depth to the distance between the passenger and grape dispenser. (C) Average normalized firing rates for the close (<1 m) distance between the passenger and observer. (D) Average normalized firing rates for the close (<1 m) distance between the passenger and grape dispenser. (E) Average flip-index for M1 (left) and PMd units (right).