Topography of Place Maps along the CA3-to-CA2 Axis of the Hippocampus

Abstract

We asked whether the structural heterogeneity of the hippocampal CA3-CA2 axis is reflected in how space is mapped onto place cells in CA3-CA2. Place fields were smaller and sharper in proximal CA3 than in distal CA3 and CA2. The proximodistal shift was accompanied by a progressive loss in the ability of place cells to distinguish configurations of the same spatial environment, as well as a reduction in the extent to which place cells formed uncorrelated representations for different environments. The transition to similar representations was nonlinear, with the sharpest drop in distal CA3. These functional changes along the CA3-CA2 axis mirror gradients in gene expression and connectivity that partly override cytoarchitectonic boundaries between the subfields of the hippocampus. The results point to the CA3-CA2 axis as a functionally graded system with powerful pattern separation at the proximal end, near the dentate gyrus, and stronger pattern completion at the CA2 end.

Neural Population Evidence of Functional Heterogeneity along the CA3 Transverse Axis: Pattern Completion versus Pattern Separation

“…The weak LEC input may seed the putative CA3 attractor bump if the LEC inputs are initially stronger than MEC, perhaps amplified by preferential connectivity to newborn dentate gyrus granule cells (Vivar et al, 2014; Neunuebel et al, 2013; Neunuebel and Knierim, 2014). Thus, in conjunction with complementary results along the CA3 transverse axis recently reported by Lu et al (in press), the present results appear to reflect a competition between inputs that is resolved in a winner-take-all manner suggestive of attractor dynamics in the network.…”

“…The CA3 activity patterns become associated with the EC inputs (heteroassociation) and with themselves through the recurrent collaterals (autoassociation). In a very well-learned environment, the associative network can create strong attractors—stable network states that are resistant to perturbation, can be self-sustaining, and can be reactivated from an initial state by weak inputs (Amit, 1989; Hasselmo et al, 1995; Knierim and Zhang, 2012; Lu et al, in press; Samsonovich and McNaughton, 1997; Treves and Rolls, 1992; Zhang, 1996). During memory retrieval, the putative CA3 attractors receive external input from both EC and DG.…”

Nonspatial sequence coding varies along the CA1 transverse axis

“…Place cell analyses were consistent with that of previous studies (e.g., Henriksen et al, 2010;Lu et al, 2015;Oliva et al, 2016), with minor parameter adjustments due to the nature of our paradigm and apparatus. The animals' location in X-Y coordinates was recorded by a behavioral tracking system using headstage-fixed LEDs at a sampling rate of 30 Hz (CinePlex, Plexon).…”

What Learning Systems do Intelligent Agents Need? Complementary Learning Systems Theory Updated

“…However, when the environment produces an input on the ERC that has low overlap with patterns stored previously, the DG recruits a new, statistically independent cell population in CA3 (i.e., pattern separation [27]). Emerging evidence suggests that the amount of overlap required for pattern completion (as well as other characteristics of hippocampal processing) may differ across the proximal-distal [145,146] and dorso-ventral axes [98,[147][148][149][150] of the hippocampus, and may be shaped by neuromodulatory factors (e.g., Acetylcholine) [85,151]. Also, incomplete patterns require less overlap with a stored pattern than distorted ones for completion to occur, so that partial cues will tend to produce completion, as when one sees the watering hole and remembers seeing a lion there previously [27].…”