The most familiar examples of conditioning focus on discrete conditional stimuli(CS—e.g., Pavlov's bell), which are present briefly and immediately before the unconditional stimulus(US-typically an electric footshock for fear conditioning). But there are also static contextual cues that are present continually throughout the entire conditioning experience. Discrete and contextual CSs share the ability for one-trial permanent conditioning[6
]. However, contextual cues do not seem to play by the same rules as discrete CSs. A ubiquitous finding in the conditioning literature is that while the best conditioning occurs with the CS starting before the US, the shorter the interval between CS onset and US onset the better the conditioning (). While the time constant differs for different types of conditioning, it is very short for eyeblink conditioning[9
] and long for taste aversion conditioning[8
], the rule is the same. The longer the time between the CS and the US the worse conditioning is, and this rule certainly applies to fear conditioning with discrete CSs[10
]. Contextual conditioning violates this rule[11
I named this violation the immediate shock deficit(ISD), although it has been documented with other aversive USs such as loud noise[12
] and several CRs[11
]. Simply put, the greater the time between placement in a novel context and the delivery of the US (placement-to-shock interval) the greater the conditioning. While simultaneous presentation of tone and shock produces robust one-trial conditioning[7
], a delay of at least 20 seconds between placement in a context and shock is needed for even minimally detectable conditioning[5
]. I proposed that this deficit arises because contexts are made of many stimulus elements that “would not be experienced until the animal engages in some exploration” and that “the pattern of stimulation would change as the animal explores the chamber”[11
]. Therefore, “the subject must learn to treat the complex compound of stimuli that make up a context as a whole …or Gestalt…before such a stimulus can enter into association as a CS”[11
]. Note that none of these requirements are present for a discrete CS—one does not need to explore a brief, simple stimulus like a tone, and all of its elements are immediately present at the time of reinforcer delivery.
The slope of the CS-US interval (placement-to-shock interval) function provides a diagnostic for elemental vs configural learning (). If that slope is negative, with conditioning degrading as CS-exposure increases, learning about the CS occurs in an elemental manner. However, if this slope is positive, where learning increases with CS exposure, learning about the CS occurs in a configural fashion. shows that the positive slope is unique to contexts. Thus we have an experimental tool for probing the nature of learning about stimuli. Later, in this article I will put this tool to use.
Further, support for this view of the context as a configuration comes from the finding that allowing the animal to form this unitary representation prior to conditioning, by simply giving it an opportunity to explore the environment, mitigates the ISD[5
]. Importantly, this pre-exposure must consist of all the context elements being present together; separately exposing the elements does not attenuate the ISD[15
]. The fact that context pre-exposure facilitates conditioning is again strikingly different than what happens with discrete CSs, where pre-exposure leads to a reduction in conditioning termed latent inhibition[16
]. Note that the context pre-exposure design is really a variant of the placement-to-shock interval experiment. Both context pre-exposure and increasing the placement-to-shock interval increases experience with the CS prior to shock. Both facilitate the formation of a configural representation of the context through experience.
If the polymodal features of the context must be linked together as a unified representation, a brain structure that processes polymodal stimuli is a likely place. Nowhere else in the brain is there a compression of multi-sensory information that rivals the hippocampus[17
]. The prediction that arises is that the hippocampus will be especially important for conditioning to contextual as opposed to discrete stimuli, because contextual but not discrete stimuli are a configuration of multisensory elements. Lesion studies confirm this prediction[18
If the hippocampus forms the contextual configure, there should be some neural signature that reflects this process. Hippocampal neurons prefer to respond in specific locations and it is thought that the relationship of firing patterns between these place neurons allows animals to distinguish one context from another[21
]. These hippocampal place fields require a period of exploration to become stable and estimates of the time needed for stability are similar to the time needed to overcome the ISD[22
]. Furthermore, just as conditioning occurs with less time between placement and shock in a pre-exposed context, hippocampal place fields stabilize more rapidly when rats are replaced in a familiar environment[22
]. Thus there is at least a rough correspondence between the temporal pattern of hippocampal place neuron activity and contextual fear conditioning.
Fear conditioning requires labeling a cue with emotional content but formation of a contextual representation by the hippocampus is independent of emotional valence. In the pre-exposure experiments, formation of the representation occurs in the absence of the US[5
]. The amygdala is a structure that has long been linked to emotion and fear conditioning[24
]. Hippocampal inputs to the basolateral amygdaloid complex (lateral and basal nuclei-BLA) support synaptic plasticity and damage to these hippocampal-BLA projections attenuates context but not tone conditioning[26
]. However, damage to neurons in the BLA attenuates both[26
shows a well-accepted view of a circuit for contextual fear that is uniquely capable of executing the requisites of this form of learning[27
]. A contextual representation is assembled in the hippocampus and this representation, like that of a simpler discrete CS, is associated with negative affect at the BLA. This gives the CS the ability to activate the BLA on its own. BLA activation descends to generate the many overt responses that constitute a fear reaction via the central nucleus. Importantly, the ventral periaqueductal gray organizes a freezing response. I say, “organize” because the initial component of freezing is to retreat to the nearest good location to freeze (e.g., the closest dark corner) and then arrest visible motor activity[29
Figure 2 Multimodal sensory information constituting the context is integrated at the hippocampus and associated with shock in the basolateral amygdala. Descending circuitry from there generates conditional responses such as freezing and analgesia. The analgesic (more ...)