Prioritization of social information by the basolateral amygdala in rats

Abstract

The amygdala is a collection of nuclei that support adaptive social behavior and are implicated in disorders such as autism. The basolateral complex of the amygdala (BLA), a main subdivision of the amygdala, influences fear responses, motivated behavior, and memory of emotional events via its communication with other amygdalar nuclei and with other brain regions such as the prefrontal cortex, striatum, and hippocampus. The specific role of the BLA in responses to social stimuli is less clear. The present study of female rats investigated the role of the BLA in responding to socially-relevant information by asking how inactivation of the BLA with bilateral infusions of the GABA receptor agonist muscimol would affect spontaneous exploration of wood blocks scented either with conspecific male or female urine or with nonsocial odorants. Conspecific urine samples were used because urine conveys information about sex, health, social status, and reproductive state in rodents. The results revealed that BLA inactivation reduced female rats' spontaneous preference for social odors over nonsocial odors, specifically for female urine. However, BLA inactivation did not generally impair rats' ability to distinguish two odors from the same category (e.g., urine odors from two different male rats). The results indicate that the BLA is important for responding to salience of social stimuli but not for discriminating between different individuals, a result that has important implications for amygdalar modulation of downstream attention, motivation, and memory processes for social stimuli.

Keywords: Affect; Amygdala; Preference; Salience; Social; Urine.

Figure 1.. Schematic diagrams of task procedures.

(A) Seven to fourteen days following surgery to implant infusion cannula bilaterally in the BLA, female rats (n=9) in cohort 1 were administered the habituation-dishabituation task and then the preference task. Female rats (n=9) in cohort 2 followed a similar timeline except that they were administered the preference task prior to the habituation-dishabituation task. (B) In the habituation-dishabituation task, 30 min following infusion of saline (Sal) or muscimol (Mus) in the BLA, female rats were presented the same odor on a clean wood block repeatedly for 5 times in a row with a 15-s interval. In the sixth presentation, rats were then presented with a new odor of the same category (male urine, female urine, or nonsocial essential oil). Two habituation-dishabituation trials were administered each testing day with an intertrial interval of approximately 1 hr, one using nonsocial odorants (N) and one using conspecific urine from either male (M) or female (F) donors. New odors were used for each trial. Spontaneous exploration times were used to infer discrimination of the repeated and new odors. (C) In the preference task, 30 min following infusion of saline or muscimol in the BLA, female rats were presented on each trial with two blocks simultaneously for 120 s, each scented with a different odor. Two trials from the same condition were administered each day with an intertrial interval of approximately 1 hr. In the first test (days 1–2), one block was scented with female urine, and one block was scented with male urine. In the second test (days 3–6), one block was scented with urine (from either a female or male donor), and one block was scented with a nonsocial essential oil. New odors were used on each trial. Spontaneous exploration times were used to infer relative preference of odors.

Figure 2.. Results from the habituation-dishabituation task (n=15).

A. The results are shown as mean exploration times across five presentations of a repeated odor and one presentation of a new odor. Squares, diamonds, and circles indicate exploration times of male urine odors, female urine odors, and plant-based nonsocial odors, respectively. Filled symbols connected by solid lines indicate data from the muscimol BLA infusion condition. Open symbols connected by dashed lines indicate data from the control saline BLA infusion condition. Female rats explored male urine more than female urine or nonsocial odors, and across all odor categories, exploration rebounded when a new odor was presented following five repetitions of the initial odor. These trends were numerically similar for both the saline and muscimol BLA infusion conditions. However, there was a significant (p<0.001) three-way interaction between odor type, odor presentation number, and infusion condition. Additionally, for female urine odors and for nonsocial odorants, there was a significant (p<0.001) two-way interaction between odor presentation number and infusion condition, as noted in the legend. B. The results for the final (5^th) habituation presentation and dishabituation (new) presentation are replotted as mean new-5 differences. There was a significant (p<0.05) two-way interaction between odor presentation number and infusion condition for the female urine odors. In both panels, the error bars represent standard errors of means. Three of the 18 rats became sick and thus did not complete testing on the habituation-dishabituation task. See sections 2.6 and 3.2 for details of analyses and results, respectively.

Figure 3.. Results from the spontaneous preference task (n=18).

Results are shown as mean preference scores indicating relative exploration of two odor categories [(X−Y)/(X+Y) * 100], for which the sign indicating the direction of change is arbitrary. Arrows adjacent to odor categories indicate the direction of change. (A) Preference scores for a test in which a block scented with female urine and a block scented with male urine were presented simultaneously. (B) Preference scores for a test which a block scented with urine (from either a female or a male donor) was presented simultaneously with a block scented with nonsocial essential oils. Inactivation of the BLA via infusion of muscimol reduced preference scores for female urine odors relative to nonsocial odors (see Section 3.2). The error bars represent standard errors of means. See sections 2.6 and 3.3 for details of analyses and results, respectively.