Electroanatomy of hippocampal activity patterns: theta, gamma waves, sharp wave-ripples, and dentate spikes

Monitoring representative fractions of neurons from multiple brain circuits in behaving animals is necessary for understanding how different brain regions interact. Using multishank, high-density recording silicon probes (up to 1,024 sites), we describe the main characteristic LFP patterns in the hippocampus, including sharp wave-ripples (SPW-Rs), dentate spikes (DSs), theta, and gamma oscillations. Our novel observations primarily relate to the distinction between subclasses of SPW-Rs and DSs, as well as their neuronal spiking correlations. In addition to the classical SPW-Rs, initiated in the CA2-3 recurrent collateral system and characterized by a large negative sharp wave (sink) in the mid-CA1 stratum radiatum (SPW-R^Rad), a small subset of ripples, associated with a sink in CA1 str. lacunosum-moleculare was also observed (SPW-R^LM). The two types of ripple events differed in frequency, magnitude, and neuronal correlates. CA3 pyramidal neurons were strongly active during SPW-R^Rad but not during (SPW-R^LM). DSs could also be grouped further based on their excitatory inputs from the medial and lateral entorhinal cortex (DS^MEC and DS^LEC), by their impact on their physiological targets, and by the brain states into which they were embedded. Overall, our experiments demonstrate the utility and need for high-density recording of both LFP and spiking activity for the appropriate classification of seemingly similar events. These distinctions relate not only to their neurogenesis but also to their behavioral-cognitive contributions.