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An Analysis of Recurrent Hippocampal Networks: Synchronization, Time, and Episodic Memory


Episodic memory is the memory of complex sequences of events; basically memories that contain information about ‘what’ occurred, ‘where’ it happened, and ‘when’. It is unclear how episodic memory is stored in the brain. The first part of this dissertation presents a model whereby the recurrent connections of hippocampal field CA3 are used to store a cue while tracking its appearance in time to allow the trace of temporally separated cues to be bound by long term potentiation (LTP). This process allows disparate elements of an episode to be linked and recovered in correct order while maintaining their temporal relationships. The proposed activities of field CA3 evident in the model were then validated by electrophysiological experiments showing that the CA3 network can produce long and broad network reverberations in vitro without the reverberation of individual pyramidal cells. Additional studies demonstrated that CA3 was required for storage of the ‘when’ component of episodic memory.

Episodic memory storage and organization happens continuously without supervision; however animals and humans use past experience to organize incoming complex information. Research described in the second part of the dissertation used exploration and learning of a complex unsupervised environment to test if prior experience with environmental complexity influenced exploration strategies and learning. We found that rats spontaneously organize their behavior into episodes and that rats with prior experience with complexity use these episodes to more efficiently explore and learn the environment as compared to rats with prior exercise or handling. Using this behavioral task we then determined where learning-related synaptic modifications occurred. Analysis of the distribution of synapses with evidence of recent LTP showed that ‘prior experience’ animals store their information in spatially discrete segments of hippocampus, and primarily in field CA1. We then used a second behavioral task to determine where episodic vs contingency-based learning was stored. We found that in the exploration paradigm, synaptic changes associated with exploration were prominent in a different collection of zones including CA1 striatum oriens and CA3c. These mapping studies reinforce the conclusion that different types or components of memory are encoded through activities of different hippocampal subfields.

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