Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Eyeblink classical conditioning is a relatively simple form of associative learning that has become an invaluable tool in our understanding of the neural mechanisms of learning. When studying rabbits in this paradigm, we observed a dramatic modification of learning rate by conducting training during episodes of either hippocampal theta or hippocampal non-theta activity as determined by on-line slow-wave spectral analysis. Specifically, if animals were given trials only when a computer analysis verified a predominance of slow-wave oscillations at theta frequencies (3–8 Hz), they learned in half as many trials as animals trained during non-theta hippocampal activity (58 vs. 115). This finding provides important evidence from awake, behaving animals that supports recent advances in our knowledge of (i) brain sites and neurobiological mechanisms of learning and memory, specifically hippocampus and theta oscillations, (ii) the biological plausibility of current models of hippocampal function that posit important roles for oscillatory potentials, and (iii) the design of interfaces between biological and cybernetic (electronic) systems that can optimize cognitive processes and performance.