*** Appendix - Higher-order associative learning in Drosophila melanogaster : a summary of research findings by Brembs and Heisenberg (2001)

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Brembs (2000) and Brembs and Heisenberg (2001) searched for certain higher-order forms of associative learning that are commonly found in vertebrates undergoing associative learning: blocking, overshadowing, sensory pre-conditioning (SPC) and second-order conditioning (SOC). The two types of conditioned stimuli used (visual patterns and colors) allowed the researchers to study the effects of compound compound stimuli and, in particular, to investigate whether overshadowing, blocking, SOC and SPC could be observed in fruit flies. Confirmation of these phenomena in Drosophila would indicate that the same laws of learning apply to both fruit flies and vertebrates.

In blocking, reinforced exposure to conditioned stimulus A alone (i.e. exposure to A followed by a US), followed by reinforced exposure to a compound stimulus AB, prevents (or blocks) the animal from responding when stimulus B is presented alone, despite its prior association with the reinforcement. In overshadowing, a stimulus that can normally condition a response when presented as a CS on its own will acquire a much weaker association with the US when presented with another, stronger, stimulus (e.g., a more intense tone or light). Thus one stimulus 'overshadows' the other. Sensory preconditioning means that reinforcement of stimulus A after unreinforced exposure to a compound AB also leads to responses to stimulus B, while second-order conditioning means that reinforcement of stimulus A followed by unreinforced exposure to a compound AB also leads to responses to stimulus B.

Of the four forms of higher-order learning, the only strong effect was for sensory pre-conditioning. Second-order conditioning was very weak. Overshadowing was inferred, while bocking was not observed, despite repeated attempts to find it. The findings are presented in detail below. The conclusion drawn is that none of the phenomena necessitates a mentalistic interpretation of Drosophila's behaviour.

Blocking was not observed in Drosophila melanogaster at the torque meter, despite careful efforts to detect it. Indeed, Brembs and Heisenberg (2001, p. 2855) reported that "We could find no unambiguous or undisputed evidence in the literature that invertebrates exhibit blocking." One salient difference between blocking experiments conducted with Drosophila and those carried out with vertebrates is the time-scale used for the training:

Whereas, in our experiments, training in the first phase of the experiment lasted for no longer than 8 min[utes], in the experiments on vertebrates it lasted for long periods, sometimes for a whole week. Vertebrates may use this extensive training to explore the situation and to generate memory templates with much higher reliability than can ever be obtained with our design. In the flight simulator, in particular, the fly with a single degree of behavioural freedom has little opportunity to explore the situation and to increase its level of 'orientedness'... In addition, 8 min[utes] in the life of a fly might well be as long as several days in the life of a rat or a pigeon. Perhaps blocking occurs only if the initial training has not only rendered the CS1 a certain or almost certain predictor of the US, but has, in addition, been stored in the memory reliably enough to render CS1 particularly difficult to extinguish during further training (Brembs and Heisenberg, 2001, p. 2854).

The alternative possibility is that invertebrates simply do not exhibit blocking. Brembs and Heisenberg (2001, p. 2855) speculate that invertebrates' memory templates are less reliable than those of vertebrates. For invertebrates, "[t]here is no reason not to remember a stimulus, even if it is only vaguely predictive for the US" (2001, p. 2855). On the other hand, vertebrates, with their larger, more complex brains, probably possess a superior ability to rapidly discern essential from redundant information, so they can afford to ignore (block) information about connections between redundant stimuli and a reinforcer (US) (Brembs, 2000, pp. 28-29). For them the costs of blocking outweigh the benefits.

Overshadowing was not directly observed, but was inferred in Drosophila from the observation that patterns and colours were learned better if trained and tested alone than if trained and tested in a compound and then tested separately. In any case, "[o]vershadowing is a well-known phenomenon in classical (e.g. James and Wagner, 1980; Rauhut et al., 1999; Rubeling, 1993; Tennant and Bitterman, 1975) and operant (e.g. Farthing and Hearst, 1970; Miles and Jenkins, 1973) conditioning in vertebrates and invertebrates (e.g. Couvillon et al., 1996; Pelz et al., 1997; Smith, 1998)" (Brembs and Heisenberg, 2001, p. 2854).

Sensory pre-conditioning (SPC) was also verified in fruit flies. In sensory preconditioning, exposure to the compound (CS1+CS2) precedes training (CS1+US). "Hence, no extinction [the process of eliminating or reducing a conditioned response by not reinforcing it - V. T.] can occur between training and testing. Flies were exposed to 16 min[utes] of unreinforced flight in which flight directions were designated by compound stimuli consisting of colours and patterns (CS1+CS2). If, immediately afterwards, one of the stimuli is paired with heat (CS1+US), the other one (CS2) is regarded as a predictor of safe and dangerous flight orientations, respectively, in the subsequent test" (Brembs and Heisenberg, 2001, p. 2854). This experiment proved that CS-US pairings are not necessary for a CS to accrue associative strength.

The second-order conditioning (SOC) effect observed was much smaller than the sensory prec-conditioning effect. The authors speculated that this may have been because in SOC, the compound (CS1+CS2) is presented after the initial training with the single stimulus (CS1+US). In the intervening period, the conditioned response observed in the flies may have time to attenuate: "the presentation of the compound without heat after the conditioning may lead to extinction of the learned association attenuating the CS1-US association (extinction)" (Brembs and Heisenberg, 2001, p. 2853).

The authors' conclusion was cautiously up-beat:

As in vertebrates, associative learning in invertebrates requires complex processing of sensory stimuli during memory acquisition. Further research is needed to determine the extent to which these processes are shared across phyla (Brembs and Heisenberg, 2001, p. 2861).

Summarising, Brembs proposes that Drosophila uses a "sophisticated, asymmetric set of rules ... [in] guiding its selection which of the predictors present in a composite learning situation are to be stored in memory for later use" (2000, p. 30).

The term "rules" might suggest that Drosophila is engaging in some kind of cognitive processing. However, in a personal email (22 December 2002), Brembs repudiated such an interpretation:

You may have noticed that I try to avoid the use of the word "cognitive". For my purposes, the distinction into cognitive and non-cognitive has no heuristic value... I personally keep a tally of tasks (in my head) of what different animals have or haven't shown to be able to successfully complete. Eventually, I want to find out how the brain solves these tasks. The question of what parts of the brain are contributing how will be answered then and the question how 'cognitive' the involved processes are, will be redundant...

Some of the above mentioned phenomena have warranted explanations that include cognition-like concepts of attention or expectation and prediction - which we discussed in the case study relating to worms, in connection with blocking. However, alternative non-cognitive interpretations are possible. Although it has been shown that some insects (e.g. Drosophila) are capable of complex learning tasks and exhibit some higher order forms of associative learning that are found in vertebrates, it has not yet been established that a first-person intentional stance or an agent-centred stance is required to explain these feats.

To sum up: it has yet to be shown that higher-order associative learning in insects requires a mind. The similarities in higher-order associative learning between insects and vertebrates do not, taken by themselves, warrant the conclusion that insects have mental states.

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