Cosyne 2007 Workshops
February 26-27, 2007
The Canyons, Utah
Sen Cheng
Experience-dependent Dynamics of Phase Precession and Coordinated Spiking
Sen Cheng and Loren M. Frank Sloan-Swartz Center for Theoretical Neurobiology and Keck Center for Integrative Neuroscience, University of California, San Francisco, CA
The hippocampus is crucial for the formation of episodic memories and the temporal organization of hippocampal neural activity like phase precession and replay during ripples are thought to be essential for binding these memories together across time. However, little is known about whether and how this organization changes to reflect the encoding of new memories. We developed a new adaptive algorithm that makes it possible to accurately describe the dynamics of phase precession during learning, and applied this to recordings of CA1 neurons from rats performing a spatial alternation task in both an entirely familiar environment and in an environment which contained one novel arm. The new model fits the data well: for approximately 70% of the neurons, the model prediction was statistically indistinguishable from the actual spike train at a 99% confidence level, as compared to less than 50% for previous adaptive models. These models can therefore be used both to analyze spatio-temporal dynamics in place cells and to simulate highly realistic place cell spike trains. When we examined the dynamics of phase precession, we found clear dynamics as a function of experience in the novel arm. Some cells showed clear phase precession on the first exposure to the novel arm, but on average the precision of phase precession was significantly lower than in the familiar environment. Phase precession in the novel arm evolved with experience, becoming more precise over 2–3 days until it was indistinguishable from that in familiar environment. The difference in theta phase precession seen on day 1 was not a result of differences in the theta rhythm or the modulation of spiking activity by theta, but rather reflected disorganization of the spatio-temporal structure of the spike train. The dynamics of phase precession were accompanied by an evolution in the synchrony of activity during ripples. On day 1, cell pairs with overlapping place fields on the novel arm fired more synchronous spikes during ripple events than did pairs with overlapping place fields in the familiar arm. Furthermore, synchronous firing diminished within 2–3 days, similar to the dynamics of phase precession. These results provide the first direct link between the dynamics of place cell activity during exploration and the dynamics of activity during the quiescent state, and suggest that synchronous activity during ripples may be important for establishing spatio-temporal organization during active exploration.
