Auditory stimuli elicit hippocampal neuronal responses during sleep

To investigate how hippocampal neurons code behaviorally salient stimuli, we recorded from neurons in the CA1 region of hippocampus in rats while they learned to associate the presence of sound with water reward. Rats learned to alternate between two reward ports at which, in 50% of the trials, sound stimuli were presented followed by water reward after a 3-s delay. Sound at the water port predicted subsequent reward delivery in 100% of the trials and the absence of sound predicted reward omission. During this task, 40% of recorded neurons fired differently according to which of the two reward ports the rat was visiting. A smaller fraction of neurons demonstrated onset response to sound/nosepoke (19%) and reward delivery (24%). When the sounds were played during passive wakefulness, 8% of neurons responded with short latency onset responses; 25% of neurons responded to sounds when they were played during sleep. During sleep the short-latency responses in hippocampus are intermingled with long lasting responses which in the current experiment could last for 1–2 s. Based on the current findings and the results of previous experiments we described the existence of two types of hippocampal neuronal responses to sounds: sound-onset responses with very short latency and longer-lasting sound-specific responses that are likely to be present when the animal is actively engaged in the task.