The flow of axonal information among hippocampal subregions: 2. Patterned stimulation sharpens routing of information transmission

The subregions of the hippocampal formation are essential for episodic
learning and memory formation, yet the spike dynamics of each region
contributing to this function are poorly understood, in part because of a
lack of access to the inter-regional communicating axons. Here we
reconstructed hippocampal networks confined to four subcompartments in 2D
cultures on a multi-electrode array that monitors individual communicating
axons. In our novel device, somal and axonal activity were measured
simultaneously with the ability to ascertain the direction and speed of
information transmission. Each subregion and inter-regional axons had
unique power-law spiking dynamics, indicating differences in computational
functions. After stimulation, spiking and burst rates decreased in all
subregions, spikes per burst generally decreased, intraburst spike rates
increased, and burst duration decreased, which were specific for each
subregion. These changes in spiking dynamics post-stimulation were found
to occupy a narrow range, consistent with the maintenance of the network
at a critical state. Functional connections between the subregion neurons
and communicating axons in our device revealed homeostatic network routing
strategies post-stimulation in which spontaneous feedback activity was
selectively decreased and balanced by decreased feed-forward activity.
Post-stimulation, the number of functional connections per array
decreased, but the reliability of those connections increased. The
networks maintained a balance in spiking and bursting dynamics in response
to stimulation and sharpened network routing. These plastic
characteristics of the network revealed the dynamic architecture of
hippocampal computations in response to stimulation by selective routing
on a spatiotemporal scale in single axons.