Distal CA1 Maintains a More Coherent Spatial Representation than Proximal CA1 When Local and Global Cues Conflict

Abstract

Entorhinal cortical projections show segregation along the transverse axis of CA1, with the medial entorhinal cortex (MEC) sending denser projections to proximal CA1 (pCA1) and the lateral entorhinal cortex (LEC) sending denser projections to distal CA1 (dCA1). Previous studies have reported functional segregation along the transverse axis of CA1 correlated with the functional differences in MEC and LEC. pCA1 shows higher spatial selectivity than dCA1 in these studies. We employ a double rotation protocol, which creates an explicit conflict between the local and the global cues, to understand the differential contributions of these reference frames to the spatial code in pCA1 and dCA1 in male Long-Evans rats. We show that pCA1 and dCA1 respond differently to this local-global cue conflict. pCA1 representation splits as predicted from the strong conflicting inputs it receives from MEC and dCA3. In contrast, dCA1 rotates more in concert with the global cues. In addition, pCA1 and dCA1 display comparable levels of spatial selectivity in this study. This finding differs from the previous studies, perhaps because of richer sensory information available in our behavior arena. Together, these observations indicate that the functional segregation along proximodistal axis of CA1 is not of the amount of spatial selectivity but that of the nature of the different inputs used to create and anchor spatial representations.

Comparable theta phase coding dynamics along the transverse axis of CA1

“…In addition, dCA1 shows higher power in LFP theta oscillations than pCA1. This work complements our earlier report that in the same experimental protocol, dCA1 and pCA1 have comparable spatial selectivity (31). These results indicate that the previously reported lower spatial selectivity and correspondingly lower theta modulation and theta phase precession in dCA1 than pCA1 (29,30) are not immutable, and experimental conditions and/or task demands may alter the balance.…”

“…Theta modulation and theta phase precession were found to be comparable between pCA1 and dCA1 for almost all cue configurations across different STD and MIS sessions. We have previously reported that dCA1 spatial representation rotates coherently with global cues from STD to MIS sessions, while pCA1 representation loses coherence (31). Loss of coherence in pCA1 can be explained by strong competing inputs it receives – MEC representation rotates with global cues (45), while distal CA3 representation rotates with local cues (46).…”

“…Spatial selectivity of the MEC/subiculum/nucleus reuniens inputs may be higher in our complex environment than in the previous simple environments. Alternatively, excitability in dCA1 may increase in response to higher task demand (31).…”

“…In contrast, neither LEC (45) nor proximal CA3 (46) show coherent rotation with global cues. We (31) proposed that in the absence of strong competing inputs, the less numerous inputs from MEC (25,45), subiculum (47–49), and nucleus reuniens (50–54) may be sufficient to drive dCA1 to rotate coherently with the global cues. While these inputs might be sufficient to explain the responses along the transverse axis of CA1 to cue mismatch, additional mechanisms must be considered to explain comparable spatial selectivity in pCA1 and dCA1 in our task (31) in contrast to the previous reports (29,30).…”

“…We (31) proposed that in the absence of strong competing inputs, the less numerous inputs from MEC (25,45), subiculum (47–49), and nucleus reuniens (50–54) may be sufficient to drive dCA1 to rotate coherently with the global cues. While these inputs might be sufficient to explain the responses along the transverse axis of CA1 to cue mismatch, additional mechanisms must be considered to explain comparable spatial selectivity in pCA1 and dCA1 in our task (31) in contrast to the previous reports (29,30). Spatial selectivity of the MEC/subiculum/nucleus reuniens inputs may be higher in our complex environment than in the previous simple environments.…”