Sublayer-Specific Coding Dynamics during Spatial Navigation and Learning in Hippocampal Area CA1

Abstract

Summary The mammalian hippocampus is critical for spatial information processing and episodic memory. Its primary output cells, CA1 pyramidal cells (CA1 PCs), vary in genetics, morphology, connectivity, and electrophysiological properties. It is therefore possible that distinct CA1 PC subpopulations encode different features of the environment and differentially contribute to learning. To test this hypothesis, we optically monitored activity in deep and superficial CA1 PCs segregated along the radial axis of the mouse hippocampus and assessed the relationship between sublayer dynamics and learning. Superficial place maps were more stable than deep during head-fixed exploration. Deep maps, however, were preferentially stabilized during goal-oriented learning, and representation of the reward zone by deep cells predicted task performance. These findings demonstrate that superficial CA1 PCs provide a more stable map of an environment while their counterparts in deeper layers provide a more flexible representation that is shaped by learning about salient features in the environment.

Impaired hippocampal place cell dynamics in a mouse model of the 22q11.2 deletion

“…No statistical methods were used to predetermine sample sizes but our sample sizes are similar to those reported in previous publications 51–53 .…”

“…Mice were surgically implanted with an imaging window over the left dorsal hippocampus, along with a steel head-post for head-fixation during the experiments as described previously 52,53 . Imaging cannulas were constructed by gluing (Norland optical adhesive) a 3-mm glass coverslip (64-0720, Warner) to a cylindrical steel cannula (3.0-mm diameter, 1.5-mm height).…”

“…Visual, auditory and olfactory stimuli were presented and all behavior signals digitized as described previously 52,53,56 . To track the linear position of the treadmill, we established three registration anchors at known positions along the belts and interpolated between them using a quadrature-encoded movement signal tied to the rotation of the treadmill wheels.…”

Degeneracy in hippocampal physiology and plasticity

“…Specifically, the role of afferent synaptic drive, local inhibition, several ion channels and receptors, dendritic spikes, spatiotemporal interactions between somatodendritic channels and receptors, and plasticity in each of these components have all been implicated in the emergence and maintenance of these codes (Bittner et al, 2015;Danielson et al, 2016;Geisler et al, 2010;Geisler et al, 2007;Grienberger et al, 2017;Harvey et al, 2009;Losonczy et al, 2010;Magee, 2001;Nakashiba et al, 2008;Nakazawa et al, 2004;Nolan et al, 2004;Royer et al, 2012;Sheffield and Dombeck, 2015;Skaggs et al, 1996;Tsien et al, 1996;Wills et al, 2005). In addition, there are lines of peer-reviewed) is the author/funder.…”

Investigation of the hippocampal information processing in freely moving rats

“…In addition, the deep and superficial sublayers of CA1 have been proposed to constitute two types of neurons, with different connectivity, spiking and oscillatory properties and possibly specialized functional roles (Bannister and Larkman, 1995;Valero et al, 2015;Danielson et al, 2016). The presence of any similar functional difference between the deep/superficial sublayers of the CA2 and CA3 regions has not been investigated.…”