Bob Kentridge 1995

Comparative Psychology: Lecture 5.

What is learned in classical conditioning?

We have discussed the processes occurring during learning by classical conditioning in some detail, however, we haven't really addressed the question of what, exactly is being learned. This is a more complicated question than it sounds. It can be divided into two parts:

Where are associations made?

In the basic classical conditioning paradigm we have four components, US, CS, UR and CR. Although the CR and UR may come to differ markedly, the initial learned response to the CS is the UR. Through what association does the CS come to elicit the UR? Initially there is a link between the US and the UR but none from the CS to the US or UR. It is quite plausible that making either association would cause the CS to elicit the UR - during training the CS is a predictor of both the US and UR (since the UR inevitably follows the US).
You'd see a Possible associations in classical conditioning image here if you were using a graphical web browser like Mosaic or Netscape.
After conditioning the CS could evoke the CR through a direct stimulus response association or it could evoke the CR indirectly through an stimulus-stimulus association with the US. In the latter case, when the CS's association with the US evokes some trace of the US in the memory of an animal, this trace, in turn evokes the UR reflexively. In the former case the CS can effectively replace the US, this hypothesis is therefore sometimes known as stimulus-substitution - Pavlov believed this was the underlying mechanism of classical conditioning. We might hope for evidence which clearly indicates that one or other of these associations underlies all classical conditioning. Evidence, however, exists to support the involvement of both types of association in classical conditioning.

Sensory-preconditioning:

  Preconditioning      Conditioning       Test
                                   
      CS2-CS1             CS1-US          CS2
The phenomenon of sensory-preconditioning supports the existence of stimulus-stimulus associations. In sensory pre-conditioning two neutral stimuli which one might use as CSs, for example a tone and a light, are repeatedly presented together without any US. One of the stimuli, CS1, is now conditioned to a US so that it elicits a CR. If the other stimulus, CS2, is now presented to the animal in the absence of the US it too elicits a CR. The only explanation can be that the animal learned an association between CS1 and CS2 during the sensory preconditioning phase of the experiment, so clearly these stimulus-stimulus associations are learnable. One cannot, however, clearly infer from this result is that the animal must have learned a stimulus-stimulus association between CS1 and the US during the conditioning phase. Both CS2-CS1-CR and CS2-CS1-US-UR associations could explain the behaviour observed. The process of second-order conditioning is, in some ways, a reversal of the sensory-preconditioning procedure. Here we start by pairing CS1 with the US. We then pair CS2 and CS1 and once again test the subject's response to CS2 alone. Again CS2 elicits a CR and again it is unclear whether this can be attributed to stimulus-stimulus or stimulus-response associations. Adding a final twist to the experiment, however, provides more conclusive evidence for stimulus-response associations.

Switching second-order conditioning USs:

	
  CS1-US1  CS2-CS1  CS1-US2  CS2-?

                        	 ?=UR1 implies S-R learning
                                 ?=UR2 implies S-S learning
Having established the association between CS2 and CS1 we now pair CS1 with a different US we now finally test the response that CS2 elicits. If conditioning is primarily a matter of learning stimulus-response associations then CS1 will become associated with the response UR1 during the first phase of the experiment and a similar CS2-UR1 association will be produced in the next phase. When CS1 is paired with the new US2 this should not effect the response produced to CS2. If, on the other hand, associations are primarily made between stimuli then the response to CS2 should change when CS1 is paired with US2 through the chain of associations CS1-CS2-UR2. In fact UR1 is produced in the final test phase of the experiment, supporting a stimulus-response model of conditioning. Notwithstanding the evidence above, there is also some evidence that classical-conditioning cannot be based solely on stimulus- response associations. It has been found that interfering with an animal's ability to make a UR during conditioning (for example by temporarily paralysing the animal with curare so that muscular URs like leg-flexion could not occur, or temporarily inhibiting salivation with atropine and so blocking part of the typical appetitive US) does not eliminate its subsequent production of a CR in response to the CS. This is quite incompatible with a simple model of CS-UR association because there is no UR to associate the CS with during conditioning. One attempt to reconcile this result with the second-order conditioning results described above is to suggest that is not the UR which becomes associated with the CS, but rather, the motivational state which to which the UR is directed. This explanation would hold that a CS becomes associated with hunger, not salivation, in an appetitive conditioning experiment and fear rather than cowering in conditioned emotional responses. This quite neatly leads us on to the question of what associations are made between?

What are associations made between?

The notion that associations might not be made to responses but to the motivational states that normally provoke those responses raises the question of whether associations in general are being made between events, that is, stimuli and responses, or between their representations in memory. Asserting that associations are made between appropriate motivational states is really just the first step towards asserting that associations are made between representations. Examining the development of CRs and the way they come to differ from URs provides evidence that associations are, at the very least, made between the motivational states associated with stimuli and responses, and not simply with the stimuli and responses themselves. So far, when I have mentioned that URs and CRs differ I have only noted subtle variations such as differences between the composition of UR and CR saliva in appetitive conditioning. Far more dramatic differences are apparent in aversive conditioning. One part of the UR to a US of electric shock is an increase in heart-rate. In a well trained animals, however, the CR they make to a CS which predicts shock is a not an increase, but a decrease, in heart-rate. Similar effects are found in CRs conditioned to drug USs. For example, if a tone is repeatedly paired with administration of analgesic doses of morphine the CR to the tone alone is not the decrease in pain sensitivity produced by morphine, but an increase in pain-sensitivity which might be thought of as compensating for the analgesic effects of morphine. These antagonistic CRs certainly fit in with a model of conditioning in which the motivational states associated with stimuli, rather than the stimuli themselves, are associated. Some more experiments on blocking take us even further towards the notion that more general representations of the qualities of stimuli are being associated. Recall that the standard blocking design involves presenting CS1 and a US during the first phase of the experiment, followed by CS1-CS2-US training in the second phase and a final CS2 alone test phase. The association of CS1 with the US during the first phase blocks the acquisition of any association between CS2 and the US in the second phase since the US is, by then, entirely predicted by CS1. Bakal, Johnson & Rescorla, performed an experiment in 1974 in which two groups correspond exactly to this simple blocking design. They added a third group of subjects who, rather than being conditioned with the same US in both training phases were conditioned with two different USs, both aversive. This change of USs had little influence on blocking, both groups failed to learn an association with CS2 during the second phase of the experiment. The explanation proffered was that, rather than learning that CS1 predicts a specific type of aversive event it became a good predictor of aversive events in general.

Bakal, Johnson & Rescorla's 1974 experiment:

  Phase 1        Phase 2            Test

                 CS1-CS2-Klaxon     CS2
  CS1-Klaxon     CS1-CS2-Klaxon     CS2
  CS1-Shock      CS1-CS2-Klaxon     CS2
One might argue that this is not so different from arguing that an association has been made between CS1 and the motivational state of fear which both USs (the klaxon and the shock) evoked. A refinement of this design by Tony Dickinson strengthens the case that associations are made with quite general properties which form parts of the representation of events rather than specific motivational states. Dickinson trained animals to expect a positive event to happen regularly (receiving some food: US+) and then showed that associating a CS with the omission of this expected nice event (CS1 in group 'a' signals that CS3 will not be followed by US+) could block learning when this CS was paired with a second CS (CS2) and an aversive US (US-) during the second phase of the experiment. The appropriate controls are ones in which CS1 is experienced with postive consequences in phase 1 (group 'b') and where CS1 has never been experience before phase 2 (group 'c').

Dickinson & Dearing's 1979 experiment:

        Phase 1           Phase 2           Test
 group

 a      CS3     US+       CS1 CS2 US-       CS2
        CS3 CS1   

        CS1 implies no US+


 b      CS3     US+       CS1 CS2 US-       CS2
        CS1     US+

        CS1 implies US+


 c      CS3     US+       CS1 CS2 US-       CS2

        CS1 is unpredictive
This result is very hard to explain in terms of association with a specific motivational state, but quite straightforward if we assume that CS1 has been associated with events having bad consequences in general.

What is learning for?

We have gone some way to answering the questions of where and what associations are made in classical conditioning. One final question - what are they for? - is probably best postponed until we have examined the other major type of animal learning - operant conditioning. A this stage I would just like to note that this question takes us right back to the heart of comparative psychology as evolutionary biology. The type of evidence we will consider concerns the differing tendencies of particular USs to become associated with different types of CSs and with variations in these tendencies across species. Similar species differences effect operant as well as classical conditioning. Before (temporarily) leaving classical conditioning it is worth noting that we have been discussing experiments performed on complex creatures like birds, rats and humans. It is also possible to demonstrate classical conditioning in much simpler organisms such as bees, cockroaches, sea-slugs and, perhaps, protozoa (which, although single-celled, have a very complex internal structure to their cell). The interesting point about the cockroaches and sea-slugs in particular is that conditioning can be demonstrated in isolated parts of their nervous systems. Leg withdrawal can be conditioned in headless cockroaches or in isolated leg and thoracic ganglion preparations (the thoracic ganglion is a much more complicated cluster of nerves in the cockroach than the brain). In the sea-slug (Aplysia) it has been possible to identify specific nerves involved in learning to make a reflexive response to a previously neutral stimulus. At this level, the only explanation of this adaptation is stimulus-substitution - activity in neurons transmitting signals from the neutral stimulus begin producing the same effect in a neuron feeding the motor- reflex as neurons signalling the US. This must be stimulus substitution. It is unwise to assume that the adaptive response to the sequence of events which constitute classical conditioning training in both sea-slugs and man are the same. In both species repeated pairing of a CS and US eventually produces a CR in response to the CS alone. In the sea-slug this is a very direct process, in the species we have been discussing in these lectures - rats, dogs, humans and so on - I hope you have seen that it is far from being so simple.

Sources.

Chapter 3 of Schwartz goes over a lot of this material and more. Tony Dickinson's 'Contemporary Animal Learning Theory' discusses the nature of associative representations, amazingly enough also in chapter 3. The facts you never knoew about conditioning in invertebrate, both intact and dissected, come from Dewsbury and Rethlingschafer which, as I mentioned before, is a great source for results like these.