Selective response of the nucleus taeniae of the amygdala to a naturalistic social stimulus in visually naive domestic chicks

Abstract

The detection of animate beings at the onset of life is important for phylogenetically distant species, such as birds and primates. Naïve chicks preferentially approach a stimulus resembling a conspecific (a stuffed fowl) over a less naturalistic one (a scrambled version of the stuffed fowl, presenting the same low-level visual features as the fowl in an unnatural configuration). The neuronal mechanisms underlying this behavior are mostly unknown. However, it has been hypothesized that innate social predispositions may involve subpallial brain areas including the amygdala. Here we asked whether a stuffed hen would activate areas of the arcopallium/amygdala complex, in particular the nucleus taeniae of the amygdala (TnA) or septum. We measured brain activity by visualizing the immediate early gene product c-Fos. After exposure to the hen, TnA showed higher density of c-Fos expressing neurons, compared to chicks that were exposed to the scrambled stimulus. A similar trend was present in the lower portion of the arcopallium, but not in the upper portion of the arcopallium or in the septum. This demonstrates that at birth the TnA is already engaged in responses to social visual stimuli, suggesting an important role for this nucleus in the early ontogenetic development of social behavior.

Figure 1

Schematic representation of the experimental apparatus. Visually naïve domestic chicks were placed in the running wheel and were free to run for 30 min towards one or the other stimuli, which were constantly rotating at the ends of the runway. The ‘stuffed fowl’ resembled the static configurations of a conspecific and the control stimulus was a ‘texture fowl’ (i.e., small pieces of an identical stuffed jungle fowl affixed in a scrambled fashion to the sides of a box). The behavior was monitored from above through a video camera and the sum of rotations in one or the other direction was recorded by an automated system.

Figure 2

An example of a coronal section showing the region of the nucleus taeniae of the amygdala (TnA) of an experimental chick. c-Fos-positive cells are stained black after the immunohistochemical procedure (red arrow) and are easily distinguishable from the c-Fos-negative cells (black arrow), which were counter stained with methyl-green.

Figure 3

Results of the brain analysis. (a) Schematic view of a coronal section showing a typical placement of the cell count zone (red rectangles) within the upper portion of the arcopallium; lower portion of the arcopallium and nucleus taeniae of the amygdala (TnA). (b) Significantly higher number of c-Fos-ir neurons is present in the TnA of the experimental chicks compared to controls (n = 8 in each condition). A similar trend is also visible in the lower portion of the arcopallium. (c) Typical placement of the cell count zone within the septum with its portioning into dorsal (SD), ventrolateral (SVL) and ventromedial (SVM) subdivisions (red lines). (d) The densities of c-Fos-ir cells in any of the septal subregions were not different between the two groups. Graph-plot: mean (black square), standard error of the mean (box) and standard deviation (whisker) (*P < 0.05). Drawings were adapted from the atlas of Kuenzel & Masson (1988). Hp = hippocampus, M = mesopallium, N = nidopallium, Str = striatum, CA = anterior commissure.