Conditioning in C. elegans is distinguishable from conditioned sensitization (alpha conditioning)
Experiments suggest that the underlying mechanism for conditioning in C. elegans - even so-called "alpha" conditioning - is different from that of non-associative learning (simple habituation and sensitization). In particular, some mutant worms have been found to be normal in tests of non-associative learning, but utterly incapable of short-term or long-term associative conditioning, unlike other, normal specimens (Morrison, Kumar, Wen, Runciman, Neghandi and van der Kooy, 1995). In the experiment which prompted this finding, C. elegans worms were conditioned to prefer one attractive chemical stimulus (Na+ ions) over another (Cl- ions) which is equally preferred under normal conditions, simply by being exposed to the former in the presence of, and the latter in the absence of, a food source (E. coli bacteria). What we have here is a case of US-US conditioning, where E.coli is the unconditioned stimulus (US) and Na+ ions represent the so-called conditioning stimulus (CS), which can also be viewed as an unconditioned stimulus, because it is attractive to C. elegans.
It was also shown that two lines of mutant worms (lrn-1 and lrn-2) do not alter their preferences after this kind of conditioning. This research appears to demonstrate that associative and non-associative learning are not only behaviourally distinct, but also genetically distinct. If this is correct, then it is inaccurate of Abramson to characterise alpha-conditioning (or US-US conditioning) as conditioned sensitization (a non-associative form of learning).
Radical changes of preferences in C. elegans
Another study (Morrison, Wen, Runciman, van der Kooy, 1999) shows that C. elegans worms can actually be conditioned to avoid a previously attractive stimulus - in other words, radically alter their preferences. Once again, lrn-1 and lrn-2 mutants show no change:
This change of preference cannot be explained away as "conditioned sensitization" because the old response is not re-awakened. The worms are actually learning to do something new: they are changing their pattern of response to a stimulus. The fact that nematode worms can be conditioned in this way indicates that they are capable of a kind of behavioural flexibility which bacteria, protoctista, plants and the simplest animals do not exhibit. According to Kilian and Muller's definition, this surely qulifies as "true" learning.
Saeki, Yamamoto and Iino (2001) report similar results, in which C. elegans worms starved for several hours on a plate containing salt (NaCl) learn to avoid the salt, which is otherwise attractive to worms. The authors write:
Summarising recent research, Rankin (personal email, 31 May 2003), whose specialty is learning in C. elegans, writes:
Abramson's cautionary remarks about the difficulties of identifying associative learning are well-taken; nevertheless, behavioural and neurological research in the last few years suggests strongly that even worms like C. elegans, with simple nervous systems, are capable of classical conditioning.
In a new olfactory associative learning paradigm, in which wild type worms learn to avoid a previously attractive diacetyl odor after it has been paired with an aversive acetic acid solution, lrn-1 and lrn-2 are impaired. Although defective in associative learning using a conditioned olfactory cue, nonassociative learning (habituation and dishabituation) using this same olfactory cue is unaffected.
This conditioning requires both the presence of NaCl and the absence of a bacterial food source, indicating that it is not merely adaptation or habituation, but that it is likely to be a form of associative learning (2001, p. 1757).
I disagree with Abramson - I believe that many invertebrates are capable of classical conditioning. Work on C. elegans with chemical cues (van der Kooy, and our context work) and thermal cues (Mori) show C. elegans can make associations between a reliable CS and a US.
*** SUMMARY of Conclusions reached