Familiarity perception call elicited under restricted sensory cues in peer-social interactions of the domestic chick.

Social cognitive mechanisms are central to understanding developmental abnormalities, such as autistic spectrum disorder. Peer relations besides parent-infant or pair-bonding interactions are pivotal social relationships that are especially well developed in humans. Cognition of familiarity forms the basis of peer socialization. Domestic chick (Gallus gallus) studies have contributed to our understanding of the developmental process in sensory-motor cognition but many processes remain unknown. In this report, we used chicks, as they are precocial birds, and we could therefore focus on peer interaction without having to consider parenting. The subject chick behavior towards familiar and unfamiliar reference peers was video-recorded, where the subject and the reference were separated by either an opaque or transparent wall. Spectrogram and behavior correlation analyses based on principal component analysis, revealed that chicks elicited an intermediate contact call and a morphologically different distress call, more frequently towards familiar versus unfamiliar chicks in acoustic only conditions. When both visual and acoustic cues were present, subject chicks exhibited approaching and floor pecking behavior, while eliciting joyful (pleasant) calls, irrespective of whether reference peers were familiar or unfamiliar. Our result showed that chicks recognized familiarity using acoustic cues and expressed cognition through modified distress calls. These finding suggests that peer affiliation may be established by acoustic recognition, independent of visual face recognition, and that eventually, both forms of recognition are integrated, with modulation of acoustic recognition

Changes of call type defined by f2−f1 frequency in different social contexts.

<p>a. Shifting distribution of f2−f1frequency in different social contexts. The series a−1 to a−6 correspond to the social contexts described in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0058847#pone-0058847-g002" target="_blank">Figure 2b</a>. The peak call number at particular f2−f1 values (kHz) is marked by arrows in each social context. Details are described in the text. b. The serial context is as follows: first, isolation; second, acoustic only exposure to unfamiliar reference chicks (v−a+); third, visual and acoustic exposure (v+a+) to unfamiliar reference chicks; fourth, a second period of isolation; fifth, v−a+ exposure to familiar chicks and sixth, v+a+ exposure to familiar reference chicks. c. Typical spectrogram of subject chick calls. D, dj and J, denote the D-call, dj-call and J-call respectively. The D-call is a “negative” expression signifying “dissatisfaction” or “distress”, the J-call is a “positive expression” signifying something “pleasant” or “joyful”, while the dj call is an intermediate call between the D and J calls. The black bar denotes 0.2 seconds.</p

Integrated analysis of social behavior towards familiar and unfamiliar reference peers by PCA.

<p>a. Subject behavior was video recorded in the v−a+ and v+a+ contexts. Seven factors were selected to differentiate responses in behavior towards familiar and unfamiliar peers after the Two sample independent t-test, and multivariate analysis by correlation matrix-based PCA (see detailed description of behavior parameters used for PCA in the text). b. The scores from the 1st and 4th component by independent PCA for v−a+ (left-upper) and v+a+ (right-upper) were approximated, with each variance ellipse by variance, co-variance-based PCA for social behavior towards familiar (Fam: black line or dotted) and unfamiliar (Unfam: grey out line or dotted) peers. The factor loading positive vectors drawn from the averaged center were adjusted three fold. Clear differences between Fam and Unfam could be seen, as Fam values distributed lower on the 4th component in the v−a+ but not v+a+ context. The direction of Fam specific distribution in the v−a+ context could be explained by the following factor loading vectors (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0058847#pone-0058847-g004" target="_blank">Figure 4a</a> and text). The statistical significance between Fam and Unfam behavior was evaluated by Wilks' lambda (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0058847#s4" target="_blank">Materials and Methods</a>). c. Call frequency of test chick towards familiar or unfamiliar reference chicks in the v−a+ and v+a+ contexts. P-values were calculated by two-sample T-test and the asterisks show significant values. Call frequency of dj calls was significantly higher towards familiar reference chicks only in the v−a+ context. However, J call frequency in the v−a+ context significantly increased relative to calls in the v+a+ context but only towards unfamiliar reference chicks.</p

Difference in the morphological variation of D calls with familiarity.

<p>a. Call type combinations from subject chicks to unfamiliar (U) and familiar (F) reference chicks. Each subject chick met an unfamiliar or familiar reference chick during this test. We counted calls from subject chicks for 30 seconds after an initial call from reference chicks. Only D- and dj-calls were observed in the v−a+ context. U(D)–F(dj) denotes meetings where the test chick emitted D-call including dj-call to unfamiliar chicks and the same chick emitted dj-calls without D-calls to familiar chicks b. The correlation plot of the call number against familiar and unfamiliar chicks in the acoustic only context. The morphological variation of U(D) calls was plotted against F(D) calls in the V−A+ context (n = 10). Here, the call frequency was higher towards familiar reference chicks. c. Comparison of D calls emitted to familiar and unfamiliar reference chicks. Each call was analyzed by Sound Analysis pro using three pairs; U(D)–U(D), U(D)–F(D) and F(D)–F(D). The error bar denotes the standard error of mean. The similarity score for U(D)–F(D) calls was significantly lower than for the other pairings by One-Way ANOVA, and Two sample independent t-test. In this analysis, we compared calls from pairs of U–U (10 pairs per session), U–F (25 pairs per session), and F–F (10 pairs per session) meetings.</p

Age- or repetition-dependent call modulation.

<p>a. Subject chick behavior was video recorded in the serial social context depicted in the left scheme (isolation and v−a+ contact). Spectrograms on the right showed typical calls produced by one subject chick on postnatal days 3, 8 and 16 (P3, 8, 16). The subject was exposed to the same reference chicks at P3, P8, and P16. Typical morphological values are indicated by serial numbers (1–5 at P3, 1–5 at P8 and 1–3 at P16). Calls emitted at P3 and P8 were defined as a “D-call”, and calls at P16 as a “dj-call”. The call type and morphology are described in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0058847#s4" target="_blank">Materials and Methods</a>. b. Modulation of call frequency differences (f2−f1 value) over developmental time. The average of five minimum values of f2−f1 (negative values, since frequency f1>f2) during behavioral tests was plotted against the test day (postnatal day). Black dots represent daily values of subject chicks meeting the same reference chicks during a test, against post natal day of development (the repeatedly-tested chicks), and red-crosses signify values of subject chicks meeting unfamiliar chicks during a test against post natal day of development (once tested chicks). The colored lines represent the respective linear regression fitted line. c. Modulation of call morphology over developmental time. The black dots represent values from repeatedly-tested chicks (see above) and red-crosses, values from once tested chicks (see above). The colored lines represent the respective linear regression fitted line.</p