Rats learn to freeze to 22-kHz ultrasonic vocalizations through autoconditioning

Rats emit ultrasonic vocalizations (USVs) at ∼22kHz and ∼50kHz, respectively, during negative and positive affective states. Among rats raised in a naturalistic social context, 22-kHz USVs serve as "alarm cries" that can elicit freezing behavior. By contrast, several studies show that naïve laboratory rats do not freeze in response to alarm cries. An obvious and consistent interpretation of these facts is that USV-elicited freezing depends on a type of social learning that ordinarily does not occur in the laboratory. However, the present study explored an alternative and explicitly non-social learning mechanism. Animals in the experimental group received multiple footshocks that elicited 22-kHz USVs. Animals in the control group were exposed to the same chamber but did not receive footshocks and, therefore, did not vocalize. When subsequently tested in a novel context, experimental animals froze in response to a novel 22-kHz USV but were unresponsive to a novel 50-kHz USV. Vocalizing during the aversive experience was predictive of subsequent freezing to the 22-kHz USV. As expected from previous studies, control animals failed to freeze to either USV. We propose that the experimental animals learned to associate their own 22-kHz USVs with an internal fear state and selectively generalized this "autoconditioning" to a novel 22-kHz USV. This non-social form of learning seems sufficiently rapid, reliable, and stimulus-specific to be ethologically adaptive.