Académique Documents
Professionnel Documents
Culture Documents
2010
REVIEWS
Gamma Oscillations in the Hippocampus Laura Lee Colgin and
Edvard I. Moser
Kavli Institute for Systems Neuroscience and Centre for the
Gamma oscillations are thought to temporally link the activity of distributed Biology of Memory, MTFS, Norwegian University of Science and
Technology, Trondheim, Norway
cells. We discuss mechanisms of gamma oscillations in the hippocampus and laura.colgin@ntnu.no
review evidence supporting a functional role for such oscillations in several key
hippocampal operations, including cell grouping, dynamic routing, and mem-
ory. We propose that memory encoding and retrieval are coordinated by
different frequencies of hippocampal gamma oscillations and suggest how
transitions between slow and fast gamma may occur.
Many cognitive operations require dynamic coor- with each theta cycle providing a discrete unit for
dination of activity across distributed groups of sensory information processing in the brain (see
neurons. Several mechanisms exist for this purpose, Ref. 44 for a review).
but one of the best understood is synchronization The second type of synchronization mechanism
of neuronal activity by oscillations. Oscillations seen in the hippocampus during alert behaviors is
can be readily studied using local field potential the relatively fast gamma oscillation (25140 Hz).
(LFP) recording techniques. LFPs are measured ex- Gamma oscillations in the hippocampus exhibit
tracellularly and, for the most part, reflect the spa- their largest amplitude when they are nested
tial integration of voltages generated by currents within the slower theta oscillations (5, 11, 49, 77).
flowing in and out of the dendrites of many neu- Although the two types of oscillatory activity often
rons within an area. When postsynaptic activity co-occur, hippocampal theta and gamma rhythms
across many cells is periodically synchronized, os- appear to be independently generated (48, 77). Un-
cillations appear in LFP recordings. Widespread like theta rhythms, which remain relatively stable
use of LFP recording techniques over the last sev- throughout active behaviors, gamma oscillations
eral decades has provided a great deal of evidence occur in bursts at particular times within the theta
suggesting that oscillations are not merely an epi- cycle (5, 12, 14, 74, 77) and have been proposed to
phenomenon but are instead important for tem- select particular cell assemblies for processing at
poral coordination of neural activity on a relatively those times (37, 38, 51, 68). Because of their high
fast time scale. frequency, gamma oscillations are ideally suited
In the hippocampus, a brain region critically for operations that require neuronal coordination
involved in encoding, storage, and retrieval of on a time scale that is beyond the range of con-
memory (75), two main types of oscillations syn- scious perception. This type of fast coordination
chronize neuronal activity during active waking may be needed during many fundamental opera-
behaviors. These two types of oscillations are tions of the hippocampus, including rapidly select-
termed theta and gamma rhythms, and their dis- ing inputs, grouping neurons into functional
tinctive temporal properties fit well with different ensembles, retrieving memories needed to cor-
coordination functions. The theta rhythm is a large rectly perform a previously learned task, and de-
amplitude, relatively slow (4 12 Hz), and highly termining which aspects of an experience will later
regular rhythm that plays an important role in be remembered. All of these processes likely in-
spatial and episodic memory processing (see Ref. volve not only activating selected cell ensembles
10 for a review). Theta rhythms in the hippocam- but also filtering out unnecessary inputs. Consis-
pus correlate with theta in many hippocampal tent with this idea, gamma oscillations in hip-
efferent and afferent structures, including the en- pocampal LFP recordings are not associated with
torhinal cortex (54), septum (59), amygdala (66), gamma-related firing in all principal neurons but
parasubiculum (30), striatum (18), and prefrontal rather only with a particular subset of neurons at a
cortex (40). Synchronized theta oscillations are given time (14, 16, 68).
well suited for connecting widespread networks of In this review, we will summarize evidence
neurons due to their 100- to 200-ms-wide period showing that gamma oscillations synchronize the
that can tolerate long conduction delays. Hip- activity of select ensembles of cells during many
pocampal theta rhythms correlate with intake of functions of the hippocampus. We will first de-
sensory information during movements such as scribe results elucidating the origins and mecha-
whisking and sniffing in rats and may temporally nisms of gamma generation in the hippocampus
segment samples of stimuli from the environment, and discuss the functional significance of these