Gamma oscillations are thought to transiently link distributed cell assemblies that are processing related information, a function that is probably important for network processes such as perception, attentional selection and memory. This 'binding' mechanism requires that spatially distributed cells fire together with millisecond range precision; however, it is not clear how such coordinated timing is achieved given that the frequency of gamma oscillations varies substantially across space and time, from approximately 25 to almost 150 Hz. Here we show that gamma oscillations in the CA1 area of the hippocampus split into distinct fast and slow frequency components that differentially couple CA1 to inputs from the medial entorhinal cortex, an area that provides information about the animal's current position, and CA3, a hippocampal subfield essential for storage of such information. Fast gamma oscillations in CA1 were synchronized with fast gamma in medial entorhinal cortex, and slow gamma oscillations in CA1 were coherent with slow gamma in CA3. Significant proportions of cells in medial entorhinal cortex and CA3 were phase-locked to fast and slow CA1 gamma waves, respectively. The two types of gamma occurred at different phases of the CA1 theta rhythm and mostly on different theta cycles. These results point to routeing of information as a possible function of gamma frequency variations in the brain and provide a mechanism for temporal segregation of potentially interfering information from different sources.

No abstract

The hippocampal local field potential (LFP) exhibits three major types of rhythms, theta, sharp wave-ripples and gamma. These rhythms are defined by their frequencies, have behavioral correlates in several species including rats and humans, and have been proposed to perform distinct functions in hippocampal memory processing. However, recent findings have challenged traditional views on these behavioral functions. Here I review our current understanding of the origins and mnemonic functions of hippocampal theta, sharp-wave ripples and gamma rhythms based on findings from rodent studies, and present an updated, synthesized view of their roles and interactions within the hippocampal network.

Progressive cognitive deficits that emerge with aging are a result of complex interactions of genetic and environmental factors. Whereas much has been learned about the genetic underpinnings of these disorders, the nature of "acquired" contributing factors, and the mechanisms by which they promote progressive learning and memory dysfunction, remain largely unknown. Here, we demonstrate that a period of early-life "psychological" stress causes late-onset, selective deterioration of both complex behavior and synaptic plasticity: two forms of memory involving the hippocampus, were severely but selectively impaired in middle-aged, but not young adult, rats exposed to fragmented maternal care during the early postnatal period. At the cellular level, disturbances to hippocampal long-term potentiation paralleled the behavioral changes and were accompanied by dendritic atrophy and mossy fiber expansion. These findings constitute the first evidence that a short period of stress early in life can lead to delayed, progressive impairments of synaptic and behavioral measures of hippocampal function, with potential implications to the basis of age-related cognitive disorders in humans.

2Neural activity was recorded from EC and CA1 of 17 rats trained to solve a simplified version of an odour-place association task thought to depend on interfacing of the hippocampus with inputs from the olfactory bulb and the piriform cortex via the EC 13-15 ( Fig. 1; Supplementary Video 1). On each trial, the animal sampled odours in a cue port for 1 s and then, depending on odour identity, ran to either of two cups for food reward (Fig. 1b). Following 3 weeks of training, the percentage of correct trials increased to asymptotic levels, reaching a criterion of two consecutive sessions of 85% correct performance after 16.8 ± 0.8 days (mean ± s.e.m; Fig. 1c; repeated measures ANOVA: F(20, 320) = 95.6, P < 0.001). Training-days number 2, 6, 10, 14 and 18 were defined as T1-T5, respectively. T5 was post-criterion for all animals.We first examined spectral activity in CA1 of 5 well-trained animals. After these animals had reached the 85% performance criterion, electrodes were implanted across the transverse axis of CA1 ( Fig. 1a; Extended Data Fig. 1a). Analyses focused on activity during the cue-sampling period, when recall of odour-place associations was expected to be initiated ( The observed 20-40 Hz coherence between LEC and CA1 could reflect disynaptic LEC-CA3 and CA3-CA1 coupling 12 . If this were the case, LEC-CA1 coherence would be expressed in both proximal CA1 (pCA1) and dCA1, considering that LEC input terminates indiscriminately along the CA3 transverse axis 13 . However, simultaneous recordings from LEC and pCA1 showed no increase in coherence during the cue interval (3 rats; Fig. 1h). At all frequencies from 13.7 to 33.2 Hz, pCA1-LEC coherence was weaker than dCA1-LEC coherence in the first group of rats (FDR corrected, q < 0.05; 12 tetrode pairs; Fig. 1i). The lack of coupling between LEC and pCA1, and between MEC and dCA1, suggests that the coherence is mediated by direct LEC-CA1 connections.We then asked whether and how oscillatory coupling between LEC and dCA1 evolves as the animals learn to use the odour cues to navigate. Tetrodes were targeted simultaneously to dCA1 and layer III of LEC in 5 rats. Once the electrodes were in place, the rats were trained to To determine whether coupling of 20-40 Hz oscillators in LEC and dCA1 is necessary for successful performance, we assessed activity at T5 on error trials ('T5e'; Supplementary Video 1).Results were compared to an identical number of correct trials from the same session (down-sampled correct trials, 'T5d'). The coherence of LEC and dCA1 oscillations in the 20-40Hz band decreased significantly on error trials ( Fig. 2a-c; paired t-test for all combinations of recording pairs, t(19) = 9.81, P < 0.001; for one pair per animal: t(4) = 5.0, P = 0.007). There was also a decrease in cross-frequency coupling in dCA1 ( Fig. 2f-g; t(9) = 6.30, P < 0.001). These findings suggest that 20-40 Hz coupling of dCA1 and LEC is necessary for successful odour-based navigation.K. M. Igarashi et al. 5The emergence of 20-40 Hz coupling was reflected in individual dCA...

The theta rhythm is one of the largest and most sinusoidal activity patterns in the brain. Here I survey progress in the field of theta rhythms research. I present arguments supporting the hypothesis that theta rhythms emerge owing to intrinsic cellular properties yet can be entrained by several theta oscillators throughout the brain. I review behavioral correlates of theta rhythms and consider how these correlates inform our understanding of theta rhythms' functions. I discuss recent work suggesting that one function of theta is to package related information within individual theta cycles for more efficient spatial memory processing. Studies examining the role of theta phase precession in spatial memory, particularly sequence retrieval, are also summarized. Additionally, I discuss how interregional coupling of theta rhythms facilitates communication across brain regions. Finally, I conclude by summarizing how theta rhythms may support cognitive operations in the brain, including learning.

No abstract

Gamma oscillations are thought to temporally link the activity of distributed cells. We discuss mechanisms of gamma oscillations in the hippocampus and review evidence supporting a functional role for such oscillations in several key hippocampal operations, including cell grouping, dynamic routing, and memory. 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.