CA1 20-40 Hz oscillatory dynamics reflect trial-specific information processing supporting nonspatial sequence memory

The hippocampus is known to play a critical role in processing information
about the temporal context in which our experiences occur. However, it
remains unclear how hippocampal oscillations are associated with
this type of information processing, and how their
functional organization is influenced by connectivity gradients.
Here we investigate these issues by examining local field
potential activity recorded across the proximodistal axis of CA1 as
rats performed a complex odor sequence memory task. More
specifically, we took advantage of the paradigm’s precise
time-locking and diverse cognitive demands to evaluate the
correspondence between specific patterns of oscillatory activity
and specific forms of information processing. Our first main
finding is that spectral content differed between behavioral states (odor
sequence processing epochs vs running epochs) and that, for each
behavioral state, the power of recruited oscillations showed
significantly distinct gradients along the proximodistal axis. Odor
sequence processing epochs were characterized by increased power in the
4-8 Hz and 20-40 Hz range, with 20-40 Hz oscillations showing a
power gradient increasing toward proximal CA1. In contrast,
running epochs were characterized by increased power in the 8-12 Hz range
and in a broad but modest increase in power across higher
frequency ranges (>24 Hz), with power gradients increasing
toward proximal and distal CA1, respectively. Our second main finding
is the discovery that 20-40 Hz oscillations were specifically and
significantly modulated by sequence memory performance. We found
that 20-40 Hz power increased with knowledge of the sequence and carried
trial-type-specific information. These results link 20-40 Hz oscillations
with trial-specific processing of nonspatial information critical for
order memory judgments, which is consistent with the demonstrated role of
the hippocampus in processing temporal relationships among events. The
prominence of such oscillations in proximal CA1 is also consistent with
evidence that medial entorhinal input is important for the processing of
temporal information in CA1.