Pavlovian conditioning, negative feedback, and blocking: mechanisms that regulate association formation.

Department of Psychologyand Brain Research InstituteUniversity of CaliforniaLos Angeles, California 90024expect to get. In Phase 2, the blocking group expecteda shock because of its prior learning about the noise.It got that shock, so it was not surprised and did notFrom accounts of the neural substrates postulated tolearn about the light. Rescorla and Wagner (1972) for-underlie memory to psychology textbook descriptions, malized this notionof surprisewitha single,veryinfluen-there is a pervasive but inaccurate perception of the tial equation that formed the basis of “US-processing”learningprocess: that associationformationresults sim- models of conditioning. Their model stated that USsply through the contiguity or pairing of events. Indeed, supported increases in associative strength propor-if one asked for a one-word description of what causes tional to the degree that they exceeded what the envi-Pavlovian conditioning, the modal response will likely ronment already predicted.SinceRescorlaand Wagner,be “pairing.” In the archetypal experiment, an arbitrary a number of very different interpretations of blockingstimulus such as a bell is paired with placement of food have been invoked, and there is still little agreementin a dog’s mouth. On the first experience with these over what is the best way to account for the phenome-stimuli the dog does little but orient toward the bell, non. One convergent line of evidence that would go abut it chews, salivates on, and swallows the food or longway towarddeciding theissuewould bethediscov-unconditional stimulus (US). Following pairing of these ery of a specific neural circuit capable of implementingstimuli the bell, now a conditional stimulus (CS), causes the type of computations called for by one of thesethedog tomoveaboutexcitedly,wagitstail,andsalivate models. Of course, such a circuit would have to be(Zener, 1937). The word “pairing” not only reflects the essential for blocking as well. Until recently, there hascasual observer’s understanding of conditioning; it is been only scant evidence for such a mechanism (Kim etalso at the core of traditional theoretical models of the al., 1998).Now, theavailable mechanisticdata supportaprocesses that cause conditioning. This view is that US-processing account of blocking.temporal contiguity, the learning theorist’s technical Thefirstsuggestionofa specificphysiologicalmecha-term for pairing, is the necessary and sufficient require- nism for blocking came from the Pavlovian fear condi-ment for the acquisition of conditional responding to tioning preparation and was based on the finding thatthe CS. At the cellular level, the mechanisms proposed fear conditioning producedananalgesic state mediatedas the neural substrates of learning, such as long-term by endogenous opioids (Bolles and Fanselow, 1980). Inpotentiation, are simply contiguity detectors. fear conditioning, an initially neutral CS is paired with aBecause it directly challenged this simple contiguity painful electric shock. The CS acquires the ability tonotion,Leon Kamin’s(1968)discoveryof a phenomenon engage anumberoffear-relatedbehaviors,one ofwhichhe labeled “blocking” is perhaps the most significant is an opioid form of analgesia (Fanselow, 1984). Sinceempirical observationabout conditioningsince Pavlov’s fear conditioningdepends on the painfulness of the US,initial descriptions. His fear conditioning experiment is an analgesic state engaged by the CS could eventuallydiagrammed in Table 1. The CS of interest was a light. diminish the reinforcingefficacy of theshock. FollowingTable 1, Phase1 would condition analgesia tothe noise.Two groups of rats received the same eight pairingsof this light with an aversive electric shock. A second During Phase 2, the light would be paired with a shockrendered ineffective by the analgesia produced by thestimulus, a white noise, was presented simultaneouslynoise.Thus, analgesia wouldprovide negativefeedbackwith the light. It is important to note that both groupson the acquisition of fear conditioning and would auto-received the exact same experience with the light andmatically perform the calculations that comprise thethey differed only with how the noise was treated. ForRescorla–Wagnermodelof conditioning(Fanselow, 1981).one group, the noise was pairedwith shock in an earlier The general form of such a negative feedback model isphase of the experiment; for the other, the noise had illustrated inFigure1. Theview isquite testablebecauseno pretraining. For the sake of simplicity, I converted theanalgesiceffectsofconditionalfeararereadilyblockedKamin’s data to show the percentage of conditioning by opioid antagonists. Initial support of this negativeobservable with the measure he used. The rats with no feedbackview was providedbythe findingthat adminis-prior experience with the noise showed near maximal tering theopioid antagonist naloxone during Phase 2 ofconditionedfear tothe light,but thosethat had received the blocking procedure attenuates blocking (Fanselownoise–shock pairings earlier exhibited almost no condi- and Bolles, 1979).tionedfear.Pretrainingtothenoise“blocked”condition- In fear conditioning,the CS and the US become asso-ing to the light. The critical point here is that despite the ciated via long-termpotentiationin theamygdala,whichfact that both groups experienced identical temporal receives information about both the neutral CS and thecontiguity between the light and shock, conditioning in painful US (Rogan etal., 1997). Outputsof theamygdalathe two groups was about as different as you could get. generate a constellation of conditional fear responses.Contiguity does not seem to be a sufficient requirement Theamygdalaisessentialforconditional analgesia (Helm-of conditioning. stetter and Bellgowan,1993). The analgesia is mediated