Conditioned turning behavior: a Pavlovian fear response expressed during the post-encounter period following aversive stimulation

Abstract

Rats were trained to fear an auditory conditioned stimulus (CS) by pairing it with a mild electric shock (the unconditioned stimulus, or US) delivered to one eyelid. After training, the CS elicited two different conditioned fear responses from rats: a passive freezing response, and an active turning response. The balance between these two modes of conditioned responding depended upon the rat's recent history of encounters with the US. If rats had not recently encountered the US, then they responded to the CS by freezing. But after recently encountering the US, rats exhibited CSevoked turning responses that were always directed away from the trained eyelid, even if the US had recently been delivered to the opposite (untrained) eyelid. This post-encounter turning behavior was not observed in rats that had been trained with unpaired presentations of the CS and US, indicating that even though CS-evoked turning was selectively expressed after recent encounters with the US, it was nonetheless a conditioned Pavlovian fear response that depended upon a learned association between the CS and US. Further supporting this conclusion, pharmacological inactivation experiments showed that expression of both freezing and turning behaviors depended upon lateralized circuits in the amygdala and periaqueductal gray (PAG) that are known to support expression of Pavlovian fear responses. These findings indicate that even though the ability of a CS to elicit Pavlovian fear responses depend upon the long-term history of CS-US pairings, the mode of conditioned responding (freezing versus turning in the present experiments) can be modulated by short-term factors, such as the recent history of US encounters. We discuss neural mechanisms that might mediate such short-term transitions between different modes of defensive responding, and consider how dysregulation of such mechanisms might contribute to clinical anxiety disorders.

Prefrontal infralimbic cortex mediates competition between excitation and inhibition of body movements during pavlovian fear conditioning

“…To investigate further the role of the IL in defensive strategy selection, we trained rats by pairing an auditory conditioned stimulus (CS; 20‐sec train of white noise pips) with an aversive unconditioned stimulus (US; unilateral periorbital shock). As reported previously (Tarpley et al, ; Halladay and Blair, , ), trained rats displayed either conditioned motor inhibition (CMI; i.e., movement suppression or freezing) or conditioned motor excitation (CME; i.e., turning in the direction away from anticipated shock), depending on whether they had recently encountered the US. CS‐evoked CMI and CME were both Pavlovian fear responses (not instrumental responses) because neither response was ever reinforced by omission of the US or the CS.…”

“…Pharmacological inactivation of either AMG or PAG has previously been shown to impair CMI and CME responses in the fear conditioning task used here (Tarpley et al, ). To investigate the contribution of the IL to CMI and CME behaviors, we pharmacologically inactivated (with MUS) or hyperactivated (with PTX) the IL.…”

“…One reason the CS failed to evoke CMI responses (as measured by R CS ) during postshock trials (Fig. A) was that, after recent encounters with shock US, rats began responding to the CS by expressing a CME response on some trials, which often included turning in the direction away from the eyelid for which shock was anticipated (Tarpley et al, ; Halladay and Blair, , ; see Fig. B).…”

“…The rat's position on the experimental platform was sampled at 30 Hz by an overhead video tracking system (Neuralynx Corporation, Bozeman, MT), which monitored the location of three light‐emitting diodes of different colors (red, blue, and green) attached to the animal's headstage for automated measurement of movement speed and turning behavior (see Tarpley et al, ; Halladay and Blair, ). Conditioned fear responses were assessed by comparing the animal's behavior during the context (CX) period, defined as the 20 sec immediately preceding CS onset, vs. the CS period, the 19 sec immediately following CS onset (the 20th pip was omitted from the CS period because the first shock pulse was delivered <1 sec after the offset of this pip).…”

“…Thus, data were analyzed from a total of 17 bilateral MUS infusions, 16 unilateral MUS infusions (because one of the MUS rats received only bilateral infusions), and 16 bilateral PTX infusions in a total of 30 rats, with no rat receiving the same infusion twice. MUS infusions were carried out both unilaterally and bilaterally to determine whether the IL's role in mediating CME is hemispherically lateralized because previous experiments in our laboratory (Tarpley et al, ) have shown unilateral effects on CME resulting from MUS infusions in both AMG and PAG. PTX was infused only bilaterally because there were no pronounced or interesting effects of unilateral MUS.…”