Classical conditioning of the eye-blink response, perhaps the best studied example of
associative learning in vertebrates, is relatively automatic and reflexive, and with the
standard procedure (simple delay conditioning), it is intact in animals with hippocampal
lesions. In delay conditioning, a tone [the conditioned stimulus (CS)] is presented just
before an air puff to the eye [the unconditioned stimulus (US)]. The US is then presented,
and the two stimuli coterminate. In trace conditioning, a variant of the standard paradigm,
a short interval (500 to 1000 ms) is interposed between the offset of the CS and the onset
of the US. Animals with hippocampal lesions fail to acquire trace conditioning. Amnesic
patients with damage to the hippocampal formation and normal volunteers were tested
on two versions of delay conditioning and two versions of trace conditioning and then
assessed for the extent to which they became aware of the temporal relationship
between the CS and the US. Amnesic patients acquired delay conditioning at a normal
rate but failed to acquire trace conditioning. For normal volunteers, awareness was
unrelated to successful delay conditioning but was a prerequisite for successful trace
conditioning. Trace conditioning is hippocampus dependent because, as in other tasks
of declarative memory, conscious knowledge must be acquired across the training
session. Trace conditioning may provide a means for studying awareness in nonhuman
animals, in the context of current ideas about multiple memory systems and the function
of the hippocampus.