Neuronal categorization and discrimination of social behaviors in primate prefrontal cortex

Abstract

It has been implied that primates have an ability to categorize social behaviors between other individuals for the execution of adequate social-interactions. Since the lateral prefrontal cortex (LPFC) is involved in both the categorization and the processing of social information, the primate LPFC may be involved in the categorization of social behaviors. To test this hypothesis, we examined neuronal activity in the LPFC of monkeys during presentations of two types of movies of social behaviors (grooming, mounting) and movies of plural monkeys without any eye- or body-contacts between them (no-contacts movies). Although the monkeys were not required to categorize and discriminate the movies in this task, a subset of neurons sampled from the LPFC showed a significantly different activity during the presentation of a specific type of social behaviors in comparison with the others. These neurons categorized social behaviors at the population level and, at the individual neuron level, the majority of the neurons discriminated each movie within the same category of social behaviors. Our findings suggest that a fraction of LPFC neurons process categorical and discriminative information of social behaviors, thereby contributing to the adaptation to social environments.

Figure 1. Behavioral task and movie stimuli.

(A) Temporal sequence of our reaction time task. (B) Clips of three types of movie stimuli in the standard set (top: two examples of grooming movies, G1, G2; middle: mounting movies, M1, M2; bottom: no-contacts movies, NC1, NC2).

Figure 2. Recording sites of G and M neurons, which are illustrated on the cortical surface of the LPFC.

The sizes of the blue, red circles indicate the numbers of G and M neurons recorded at each site, respectively. Black dot, recording sites without G and M neurons. The right inset shows a diagram of brain areas . AS, arcuate sulcus. PS, principal sulcus. BA, Brodmann area.

Figure 3. Examples of G and M neurons.

(A) An example of a G neuron in which the activity in grooming movies was significantly different in comparison with the others. Movie clips, raster displays and averaged histograms for neuronal activity are shown according to the type of social behaviors. F, fixation period. M, movie period. (B) An example of an M neuron in which the activity in mounting movies was significantly different in comparison with the others. The format and abbreviations are the same as those in Fig. 3A.

Figure 4. An example of an M neuron tested with the standard set and the confirmation set of movies.

The format and abbreviations are the same as those in Fig. 3A.

Figure 5. Examples of G and M neurons’ responses to mosaic movies and scrambled movies.

(A) Examples of the activity of G and M neurons for original and mosaic stimuli. (B) Examples of the activity of G and M neurons for original and scrambled stimuli. The format and abbreviations are the same as those in Fig. 3A.

Figure 6. Population normalized-activities of G and M neurons.

Population histograms of (A) G (n  = 94) and (C) M (n  = 14) neurons were aligned at the movie start. G1 (G2), the activity for the G1 (G2) movie. G, the averaged activity for two grooming-movies. M1 (M2), the activity for the M1 (M2) movie. M, the averaged activity for two mounting-movies. NC, the averaged activity for two no-contacts-movies. Mean normalized activities (mean ± S.E.) of (B) G and (D) M neurons during the whole movie period are shown. *, P<0.05.

Figure 7. Population normalized-activities of G and M neurons tested with both the standard and the confirmation sets of movies.

Mean normalized activities (mean ± S.E.) of (A) G (n  = 15) and (B) M (n = 3) neurons during the whole movie period are shown. NC, the averaged activity for the no-contacts movies. G, the averaged activity for the grooming movies conducted by two monkeys. M, the averaged activity for the mounting movies. G3, the averaged activity for the movies of grooming conducted by three monkeys. GS, the averaged activity for the movies of self-grooming of plural monkeys. *, P<0.05.

Figure 8. Quantitative analyses of the neuronal categorization of social behaviors.

(A) For G and M neurons, average between-category differences (BCDs) and average within-category differences (WCDs) are shown. (B) For G and M neurons, social-behavior categorization index (SCI) values that were computed from BCD and WCD are shown. Positive values of indices indicate larger differences for movies in different categories and negative values indicate larger differences within each category.

Figure 9. Comparison of the degree of the neuronal categorization in discriminative and categorical sub-types of G and M neurons.

For G and M neurons, (A) distribution and (B) mean (± S.D.) of social-behavior categorization index (SCI) values that were computed by each sub-type of neurons are shown. White bar (Cat): categorical sub-type neuron, gray bar (Dis): discriminative sub-type neuron. *, P<0.05.