Fear Conditioning by Proxy: Social Transmission of Fear Between Interacting Conspecifics

Abstract

We describe a method of social fear transmission to a discrete auditory cue in freely behaving rats. Extending beyond traditional observer/demonstrator paradigms, rats are allowed to physically interact and integrate cues from all sensory modalities. In the protocol described in this article, "observer" rats experience social fear conditioning through a proxy cage mate that serves as a "demonstrator" during retrieval of a cued fear memory. We find that a specific auditory cue can come to elicit fear expression in an animal with no foot shock experience simply by interacting with a conspecific expressing a conditioned response in the presence of an otherwise benign stimulus. In this "fear conditioning by proxy" paradigm, we have demonstrated that some, but not all, rats display conditioned responding (e.g., freezing) to a cue after interacting with a cage mate during fear memory retrieval. The amount of freezing exhibited by this fear conditioned "by proxy" rat 24 hr after learning critically depends on social influences, including social relationships and social interactions during learning. © 2018 by John Wiley & Sons, Inc.

Observational Fear Learning in Rats: Role of Trait Anxiety and Ultrasonic Vocalization

“…The present study investigated the role of trait anxiety and ultrasonic vocalization on observational fear learning in rats. For our experiments, we used a published protocol [33] in which rats from the same cage were grouped in triads (DEM, OBS, NAIVE). The DEM rat was directly fear-conditioned, the OBS rat had to learn fear by observing the DEM rat, and the NAIVE rats stayed naive until the fear retention test.…”

“…In these studies, rats learned fear by observation, i.e., they joined an already fear-conditioned conspecific (the "demonstrator") in a retention session on conditioned fear and could observe its fear responses to the conditioned context and/or discrete stimulus (that are neutral for the observer rat). To test whether fear was acquired by observation, a further retention test was performed one day later in which the observer rat alone was exposed to the conditioned context or stimulus [33]. Observational fear learning has been successful in male and female cage-mates [30,32], was more pronounced in related and submissive rats [31,32] and less pronounced in dominant rats [31].…”

“…In the present study, the role of trait anxiety and ultrasonic vocalization on observational fear learning in male Wistar rats was investigated. Two experiments using a published protocol [33] were performed: In the first experiment, trait anxiety was assessed in the light-dark box test before the rats were submitted to the observational fear learning procedure. In the second experiment, ultrasonic vocalization was recorded throughout the whole observational fear learning procedure and 22 kHz and 50 kHz calls were analyzed.…”

Direct and Indirect Measurements of Sex Hormones in Rodents During Fear Conditioning

“…Other systems use video‐tracking of the animal for later frame‐by‐frame analysis to determine the lack of movement or use infrared light beams to detect freezing, among others. It is beyond the scope of this article to describe how to measure freezing during FC; to that end, you can consult other protocols (see Current Protocols articles; Chang et al., 2009; Jones, Agee, & Monfils, 2018; Pickens, Golden, & Nair, 2013).…”

“…Other systems use video-tracking of the animal for later frame-by-frame analysis to determine the lack of movement or use infrared light beams to detect freezing, among others. It is beyond the scope of this article to describe how to measure freezing during FC; to that end, you can consult other protocols (see Current Protocols articles; Chang et al, 2009;Jones, Agee, & Monfils, 2018;Pickens, Golden, & Nair, 2013). This procedure is typically carried out inside a fear chamber (Basic Protocol 1), approximately 25 × 25 × 25 cm in size, that is equipped with a speaker on the ceiling or the walls that provides tones as well as white noise and with a lightbulb that may dispense visual light cues.…”