• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of nihpaAbout Author manuscriptsSubmit a manuscriptNIH Public Access; Author Manuscript; Accepted for publication in peer reviewed journal;
Curr Opin Neurobiol. Author manuscript; available in PMC Apr 1, 2011.
Published in final edited form as:
PMCID: PMC2862842
NIHMSID: NIHMS188929

Synchronous Neural Activity and Memory Formation

Summary

Accumulating evidence suggests that the synchronization of neuronal activity plays an important role in memory formation. In particular, several recent studies have demonstrated that enhanced synchronous activity within and among medial temporal lobe structures is correlated with increased memory performance in humans and animals. Modulations in rhythmic synchronization in the gamma- (30–100 Hz) and theta-frequency (4–8 Hz) bands have been related to memory performance, and interesting relationships have been described between these oscillations that suggest a mechanism for inter-areal coupling. Neuronal synchronization has also been linked to spike timing-dependent plasticity, a cellular mechanism thought to underlie learning and memory. The available evidence suggests that neuronal synchronization modulates memory performance as well as potential cellular mechanisms of memory storage.

Introduction

Ever since Donald Hebb formulated the theory that changes in the strength of neuronal connectivity follow from the correlated activation of multiple neurons [1] the study of memory has been closely tied to the study of synchronous activity in the brain. The discovery that concurrent activation of presynaptic and postsynaptic neurons can lead to long-lasting changes in signal transmission [2] has produced an entire field of study. Central to these studies is the concept that the precise synchronization of neuronal activity is one of the underlying mechanisms by which information is stored in neural tissue. This phenomenon has been well-characterized at the level of single neurons, and growing evidence suggests that precisely timed neuronal activity at the network level can be linked to improved memory performance.

As documented in a recent review [3], significant advances have been made in our understanding of spike timing-dependent plasticity (STDP), which involves changes in synaptic connectivity induced by the precise timing of spiking activity of multiple neurons in relation to one another. The ability of synchronized activity between two neurons to induce long-term potentiation (LTP) or long-term depression (LTD) of the synapse(s) connecting those neurons depends on whether the activity falls within a particular critical window (10–20 ms), as well as whether the presynaptic spike precedes or follows the postsynaptic spike within this window [48]. The size of the window varies depending on the cell type as well as the dendritic location of intercellular connections [912]. Because LTP and LTD can lead to long-lasting changes in neuronal properties, including receptor trafficking and spine motility, these studies provide a direct link between synchronous neuronal firing and the modifications that may underlie memory formation in the brain.

In this article we review evidence, gathered over the past two years, that synchronization of neuronal activity in the brain can affect memory formation. The results from these studies have furthered the idea that gamma- (30–100 Hz) and theta- frequency (4–8 Hz) synchronization, and the interaction between these two rhythms, may engender the critical conditions by which synchrony among neural networks can support the specific processes underlying learning at the cellular level in the brain.

Gamma-band oscillations link memory formation to cellular mechanisms of learning

Neuronal ensembles often synchronize their activity at particular frequencies, producing oscillations that can be measured either noninvasively or with subdural arrays or electrodes planted deep within the brain. Modulations in oscillatory activity are often seen as humans and animals engage in cognitive tasks. Gamma-band oscillations, in particular, have been associated with neuronal processing when the brain is in an “active” state, such as during attentional or mnemonic processing [1315]. In the hippocampus, gamma-band oscillations rely on interactions between inhibitory networks and local collaterals of pyramidal cells providing excitatory signals to the network ([16]; see [17] for a recent review on the generation of gamma-band oscillations in hippocampal area CA3). Gamma-band synchronization may affect signal transmission by two distinct mechanisms. First, gamma-band synchronization may provide input gain modulation through the influence of rhythmic network inhibition on local principal cells. Because these oscillations arise from strong, perisomatic inhibition from networks of local interneurons [1718], the efficacy of excitatory input to neurons within the oscillating network is highest when this input arrives out of phase with this rhythmic inhibition. In this way, gamma-band oscillations can align rhythmic inhibition among neuronal groups, ensuring that the interactions between groups are the strongest when their phases are well-aligned with each other [19; Figure 1]. Second, neurons under the common influence of gamma-band oscillation will tend to fire within 10 ms of each other (roughly the equivalent of a gamma-band half-cycle). This synchronization may enhance the impact of multiple excitatory neurons to downstream areas, where they converge on a common target. This feedforward coincidence detection may involve increased temporal summation of excitatory postsynaptic potentials, resulting in an increased likelihood that downstream neurons will fire. In this way, gamma-band oscillations may serve to enhance the impact of projection neurons [2022]. As mentioned above, correlated activity within this time window (10–20 ms) is a necessary condition for STDP. Accordingly, gamma-band oscillations may promote interactions among neurons that bring about the synaptic changes thought to be necessary for memory formation.

Figure 1
Gamma-band synchronization in the medial temporal lobe during memory encoding is associated with the degree of subsequent recognition

Although much research has focused on the role of gamma-band synchronization in selective attention [2326], many recent studies have observed synchronous activity in the medial temporal lobe (MTL) during performance of memory tasks in rodents [2729], humans [14,3039], and most recently in monkeys [40]. Changes in neuronal activity have been observed, with respect to memory formation, in oscillatory power, which reflects the energy per unit time within a particular frequency range, and coherence, which is a measure of linear predictability that captures phase and amplitude correlations. In particular, studies of intracranial electroencephalography (iEEG) signals in human epileptic patients have shown that when subjects study lists of words and are subsequently asked to freely recall as many words as possible, gamma-band power in the MTL is higher during the encoding of subsequently recalled words then unrecalled words [39]. Using a similar task, others showed that gamma-band coherence between iEEG signals in the hippocampus and the rhinal cortex also predicts successful memory encoding [14,32].

Recently, the relationship between gamma-band synchronization and memory formation was extended to single hippocampal neurons. Monkeys were shown a series of novel pictures which were repeated after a variable delay, and recognition for the pictures was inferred based on the time spent looking at pictures during the repeated presentation relative to the initial presentation. Hippocampal neurons showed enhanced gamma-band coherence with each other and with simultaneously-recorded local field potentials (LFPs) during stimulus encoding in a manner that predicted the degree of subsequent recognition [40]. The time-course of this enhancement was extremely similar in monkeys and humans, using different behavioral paradigms, suggesting that gamma-band synchronization may reflect a basic mechanism for the neuronal interactions that are critical for successful memory encoding (Figure 1).

Coupling between gamma-band and theta-band oscillations

Modulations in gamma-band oscillations are often observed with respect to the phase of slower oscillations. This has primarily been observed in the theta-frequency band [4143], but instances of cross-frequency coupling with the alpha-frequency (8–13 Hz) band have also been noted [44]. For example, Canolty and colleagues found that power in the fast gamma-frequency (80–150 Hz) band was highest at the trough of the theta-band oscillation in the human electrocorticogram [42]. Cross-frequency coupling may represent a mechanism for inter-areal communication. In support of this idea, it was recently observed that gamma-band oscillations in hippocampal area CA1 of the rat hippocampus can be divided into fast and slow components, each occurring at a particular phase of the theta-band oscillation, and each associated with a different source of afferent input to CA1 [45]. Slow (~25–50) gamma-band oscillations in CA1 were most prominent during the descending phase of the theta-band oscillation and were synchronous with slow gamma-band oscillations in CA3, while fast (~65–150) gamma-band oscillations in CA1 peaked during the trough of the theta-band oscillation and synchronized with fast gamma-band oscillations in medial entorhinal cortex. These results suggest that hippocampal theta-band oscillations may play a role in regulating information flow from entorhinal cortex and CA3 to CA1 in a way that optimizes memory encoding and retrieval. Also, similar to results obtained in monkey hippocampus for gamma-band synchronization [40], spike-field coherence in the theta-band is enhanced during the encoding of visual stimuli in human hippocampus (A Rutishauser et al., abstract in Soc Neurosci Abstr 2009, 622.4). The hippocampal theta-band oscillation has been shown to exert an influence over activity in other areas of the cortex, as well. In one recent study, neurons in primary sensory cortices and the medial prefrontal cortex were transiently coherent with locally-generated gamma-band oscillations during exploration or REM sleep, and “bursts” of gamma-band oscillations as well as with theta-band oscillations generated in the hippocampus [46]. Taken together, these findings support the idea that rhythmic modulation in the gamma- and theta-frequency bands interact in support of memory formation and that theta-band phase can convey important information about the flow of information in the MTL during encoding processes [47].

Phase resetting as a mechanism of processing during memory formation

Because the phase of the theta-band oscillation can have important implications for gamma-band oscillations, gamma-band coherence, and thus memory formation, it is important to consider behavioral factors that may influence theta-band phase at any given moment. During working memory tasks, stimulus presentation induces shifts in the phase of the hippocampal theta-band oscillation [4849]. Such phase-resetting has recently been studied in monkey visual and auditory cortices [5051], where it appears to play a role in modulating neuronal responses to incoming sensory stimuli. Particularly noteworthy in this regard is the finding that oscillations in monkey primary auditory cortex undergo phase-reset upon somatosensory stimulation [51]. This modulation affected the neuronal response to auditory stimuli such that auditory inputs arriving at a specific phase of the low-frequency oscillation produced an amplified neuronal response. Interestingly, similar effects have been seen in monkey primary visual cortex with respect to eye movements. Theta-band phase reset occurs upon fixation onset when monkeys make saccades in complete darkness, and the oscillatory phase at stimulus onset determines the strength of the subsequent neural response [50]. Such phenomena are thought to represent a mechanism by which salient events (e.g. saccades or microsaccades [50,52]) trigger a reset in ongoing oscillatory activity to an “ideal phase” in order to optimize the processing of incoming information. Similarly, theta-band oscillations in the monkey hippocampus undergo phase reset upon stimulus presentation as well as fixation onset (MJ Jutras & EA Buffalo, abstract in Soc Neurosci Abstr 2009, 480.2). If theta-band phase influences the patterns of signaling in the MTL through modulations in the power of gamma-band oscillatory activity, as seen in other systems [4142], then resetting to an ideal phase upon salient environmental or behavioral events may set different regions of the MTL to the optimum state of synchronization for memory formation and retrieval. Because LTP is optimally induced at particular phases of the theta-band oscillation in the hippocampus [5355], hippocampal theta-band phase-resetting may also have important implications for memory formation through enhanced plasticity. These various mechanisms associated with theta-band oscillations, and their proposed role in memory formation, are summarized in Box 1. Interestingly, other recent evidence indicates that the amplitude of theta-band oscillations in the human MTL even before stimulus encoding can predict subsequent recognition [38], suggesting that oscillatory activity may play an important functional role in generating a cognitive state associated with successful memory formation.

Box 1
Memory-related mechanisms associated with theta-band oscillatory activity

Conclusion

In conclusion, there have been a number of recent advances in our understanding of the role of synchronized neuronal activity in memory formation. Several recent studies have shown gamma-band neuronal synchronization during the encoding of sensory information, and that subsequent memory formation can be predicted by in the magnitude of this synchronization, both within and between regions of the medial temporal lobe. There have been clear demonstrations of interactions across frequency bands, particularly between the theta- and gamma-frequency bands, and an important topic of future research will be to further elucidate the functional implications of these interactions. Intriguing new findings have provided evidence for behavioral conditions that can control oscillatory phase-resetting, thereby modulating neuronal synchronization as well as sensory processing. However, the behavioral outcome of this kind of modulation has yet to be demonstrated. For the most part, findings regarding the functional implications of enhanced synchronization are still correlational, and future studies that may involve experimentally enhancing or reducing synchronization, perhaps by taking advantage of modulations in phase resetting, will be critical for advancing our understanding of the role of synchronous neuronal activity in learning and memory.

Acknowledgments

This work was supported by the Yerkes National Primate Research Center through base grant RR00165 from the National Institutes of Health, Emory Alzheimer’s Disease Research Center grant AG025688 (E.A.B.), the NIGMS (M.J.J.), and grants from the National Institute of Mental Health, MH080007 (E.A.B.) and MH082559 (M.J.J.).

Footnotes

Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

References

Papers of particular interest, published within the period of review, have been highlighted as:

• of special interest

•• of outstanding interest

1. Hebb DO. The organization of behavior; a neuropsychological theory. New York: Wiley; 1949.
2. Bliss TV, Lomo T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. Journal of Physiology. 1973;232:331–356. [PMC free article] [PubMed]
3. Caporale N, Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annual Review of Neuroscience. 2008;31:25–46. [PubMed]
4. Zhang LI, Tao HW, Holt CE, Harris WA, Poo M. A critical window for cooperation and competition among developing retinotectal synapses. Nature. 1998;395:37–44. [PubMed]
5. Levy WB, Steward O. Temporal contiguity requirements for long-term associative potentiation/depression in the hippocampus. Neuroscience. 1983;8:791–797. [PubMed]
6. Bi GQ, Poo MM. Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. Journal of Neuroscience. 1998;18:10464–10472. [PubMed]
7. Debanne D, Gahwiler BH, Thompson SM. Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. Journal of Physiology. 1998;507 ( Pt 1):237–247. [PMC free article] [PubMed]
8. Markram H, Lubke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science. 1997;275:213–215. [PubMed]
9. Rao RP, Sejnowski TJ. Spike-timing-dependent Hebbian plasticity as temporal difference learning. Neural Computation. 2001;13:2221–2237. [PubMed]
10. Froemke RC, Poo MM, Dan Y. Spike-timing-dependent synaptic plasticity depends on dendritic location. Nature. 2005;434:221–225. [PubMed]
11. Sjostrom PJ, Hausser M. A cooperative switch determines the sign of synaptic plasticity in distal dendrites of neocortical pyramidal neurons. Neuron. 2006;51:227–238. [PubMed]
12. Letzkus JJ, Kampa BM, Stuart GJ. Learning rules for spike timing-dependent plasticity depend on dendritic synapse location. Journal of Neuroscience. 2006;26:10420–10429. [PubMed]
13. Gruber T, Tsivilis D, Montaldi D, Muller MM. Induced gamma band responses: an early marker of memory encoding and retrieval. Neuroreport. 2004;15:1837–1841. [PubMed]
14. Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger CE, Fernandez G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nature Neuroscience. 2001;4:1259–1264. [PubMed]
15. Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR. Theta and gamma oscillations during encoding predict subsequent recall. Journal of Neuroscience. 2003;23:10809–10814. [PubMed]
16. Csicsvari J, Jamieson B, Wise KD, Buzsaki G. Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron. 2003;37:311–322. [PubMed]
17. Hajos N, Paulsen O. Network mechanisms of gamma oscillations in the CA3 region of the hippocampus. Neural Networks. 2009;22:1113–1119. [PubMed]
18. Papp E, Leinekugel X, Henze DA, Lee J, Buzsaki G. The apical shaft of CA1 pyramidal cells is under GABAergic interneuronal control. Neuroscience. 2001;102:715–721. [PubMed]
19. Womelsdorf T, Schoffelen J-M, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P. Modulation of neuronal interactions through neuronal synchronization. Science. 2007;316:1609–1612. [PubMed]
20. Konig P, Engel AK, Singer W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends in Neurosciences. 1996;19:130–137. [PubMed]
21. Salinas E, Sejnowski TJ. Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. Journal of Neuroscience. 2000;20:6193–6209. [PubMed]
22. Salinas E, Sejnowski TJ. Correlated neuronal activity and the flow of neural information. Nature Reviews Neuroscience. 2001;2:539–550. [PMC free article] [PubMed]
23. Fries P, Reynolds JH, Rorie AE, Desimone R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science. 2001;291:1560–1563. [PubMed]
24. Fries P, Womelsdorf T, Oostenveld R, Desimone R. The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4. Journal of Neuroscience. 2008;28:4823–4835. [PMC free article] [PubMed]
25. Womelsdorf T, Fries P, Mitra PP, Desimone R. Gamma-band synchronization in visual cortex predicts speed of change detection. Nature. 2006;439:733–736. [PubMed]
26. Taylor K, Mandon S, Freiwald WA, Kreiter AK. Coherent Oscillatory Activity in Monkey Area V4 Predicts Successful Allocation of Attention. Cerebral Cortex. 2005;15:1424–1437. [PubMed]
••27. Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, Stead M, Abbott LF, Kandel ER. Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biology. 2009;7:e1000140. This study addresses the role of selective attention in the physiological mechanisms underlying the formation of hippocampal place fields, which are displayed by neurons that fire preferentially when the animal is in a particular spatial location. Mice were trained to perform two different versions of a goal-oriented task: one involving learning visuospatial associations between a location and a reward, and another involving non-spatial associations between an odor and a reward. Mice trained in the visuospatial task displayed long-term stable, organized place fields in hippocampal area CA1, while mice trained in the non-spatial odor task did not, despite equal levels of learning for both groups. In addition, there was an increase in coherence between hippocampal spiking activity and slow gamma-band (20–60 Hz) local field potential activity during search only for animals that attended the visuospatial environment, and this increase in synchonization was correlated with the increase in place field stability. [PMC free article] [PubMed]
28. Jeewajee A, Lever C, Burton S, O’Keefe J, Burgess N. Environmental novelty is signaled by reduction of the hippocampal theta frequency. Hippocampus. 2008;18:340–348. [PMC free article] [PubMed]
29. Montgomery SM, Buzsaki G. Gamma oscillations dynamically couple hippocampal CA3 and CA1 regions during memory task performance. Proceedings of the National Academy of Sciences of the United States of America. 2007;104:14495–14500. [PMC free article] [PubMed]
30. Jacobs J, Kahana MJ, Ekstrom AD, Fried I. Brain oscillations control timing of single-neuron activity in humans. Journal of Neuroscience. 2007;27:3839–3844. [PubMed]
31. Jensen O, Kaiser J, Lachaux JP. Human gamma-frequency oscillations associated with attention and memory. Trends in Neurosciences. 2007;30:317–324. [PubMed]
32. Fell J, Klaver P, Elfadil H, Schaller C, Elger CE, Fernandez G. Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization? European Journal of Neuroscience. 2003;17:1082–1088. [PubMed]
33. Fell J, Ludowig E, Rosburg T, Axmacher N, Elger CE. Phase-locking within human mediotemporal lobe predicts memory formation. NeuroImage. 2008;43:410–419. [PubMed]
34. Fell J, Fernandez G, Klaver P, Axmacher N, Mormann F, Haupt S, Elger CE. Rhinal-hippocampal coupling during declarative memory formation: dependence on item characteristics. Neuroscience Letters. 2006 [PubMed]
35. Fell J, Klaver P, Elger CE, Fernandez G. The interaction of rhinal cortex and hippocampus in human declarative memory formation. Reviews in the Neurosciences. 2002;13:299–312. [PubMed]
36. Mormann F, Osterhage H, Andrzejak RG, Weber B, Fernandez G, Fell J, Elger CE, Lehnertz K. Independent delta/theta rhythms in the human hippocampus and entorhinal cortex. Frontiers in Human Neuroscience. 2008;2:3. [PMC free article] [PubMed]
37. Mormann F, Fell J, Axmacher N, Weber B, Lehnertz K, Elger CE, Fernández G. Phase/amplitude reset and theta-gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus. 2005;15:890–900. [PubMed]
•38. Guderian S, Schott BH, Richardson-Klavehn A, Duzel E. Medial temporal theta state before an event predicts episodic encoding success in humans. Proceedings of the National Academy of Sciences of the United States of America. 2009;106:5365–5370. This study used magnetoencephalographic (MEG) recordings to examine brain activity in human subjects as they studied lists of words using either deep (“pleasant” or “unpleasant”) or shallow (syllable counting) processing. Following a distracter task, subjects were asked to recall as many study words as possible during a 90-s free-recall test. The amplitude of theta-band oscillations was significantly higher for later recalled words than for later forgotten words starting around 200 ms before, and lasting until, stimulus onset, regardless of the level of processing involved. Source analysis revealed sources of pre-stimulus theta-band activity bilaterally in the MTL. [PMC free article] [PubMed]
39. Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, Tully MS, Kahana MJ. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cerebral Cortex. 2007;17:1190–1196. [PubMed]
••40. Jutras MJ, Fries P, Buffalo EA. Gamma-band synchronization in the macaque hippocampus and memory formation. Journal of Neuroscience. 2009;29:12521–12531. In this study of recognition memory signals in the hippocampus, monkeys viewed 200 novel, complex images, which were then repeated after a variable delay period. Stimuli were ranked by the reduction in looking time from first to second presentation, as a proportion of the looking time during the first presentation. Stimuli with the largest reduction in looking time were classified as being well-remembered. Gamma-band spike-spike coherence, spike-field coherence, and LFP power were significantly enhanced during the encoding of these stimuli compared to the encoding of stimuli that were poorly remembered, despite the absence of a significant relationship between encoding strength and firing rate during novel stimulus presentation. There was also no significant correlation when the same stimuli were ranked in terms of absolute looking time during novel presentation, suggesting that interest or attention was not a factor in this relationship. [PMC free article] [PubMed]
41. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. An Oscillatory Hierarchy Controlling Neuronal Excitability and Stimulus Processing in the Auditory Cortex. Journal of Neurophysiology. 2005;94:1904–1911. [PubMed]
42. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT. High gamma power Is phase-locked to theta oscillations in human neocortex. Science. 2006;313:1626–1628. [PMC free article] [PubMed]
43. Jensen O, Colgin LL. Cross-frequency coupling between neuronal oscillations. Trends in Cognitive Sciences. 2007;11:267–269. [PubMed]
44. Osipova D, Hermes D, Jensen O. Gamma power is phase-locked to posterior alpha activity. PLoS One. 2008;3:e3990. [PMC free article] [PubMed]
••45. Colgin LL, Denninger T, Fyhn M, Hafting T, Bonnevie T, Jensen O, Moser MB, Moser EI. Frequency of gamma oscillations routes flow of information in the hippocampus. Nature. In press. In this study, activity was recorded from the hippocampus and layer 3 of medial entorhinal cortex (MEC) in rats as they foraged in an open field enclosure. Gamma-band oscillations recorded in area CA1 of hippocampus split into two distinct components, each of which was associated with a different phase of the underlying theta-band oscillation. Slow (~25–50 Hz) gamma episodes peaked during the descending phase of hippocampal theta, while fast (~65–140 Hz) gamma episodes peaked during the trough of theta. In addition, coherence between areas CA3 and CA1 was pronounced in the slow gamma-band, and the firing patterns of 53% of CA3 neurons were significantly phase-locked to CA1 slow gamma; conversely, coherence between MEC and CA1 was higher in the fast gamma-band, and 44% of MEC neurons were significantly phase-locked to CA1 fast gamma.
•46. Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsaki G. Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron. 2008;60:683–697. This study provides direct evidence that cell assemblies outside of the limbic system are under the influence of hippocampal theta oscillations. Chronic recordings from rats and mice were made either during elevated maze exploration or REM sleep. A percentage of neurons throughout associative and primary sensory cortices and medial prefrontal cortex preferentially fired during particular phases of the hippocampal theta oscillation. There were transient increases in gamma-band spike-field coherence and LFP power in these neocortical areas, and these were also modulated by the phase of hippocampal theta. [PMC free article] [PubMed]
47. Hasselmo ME, Bodelon C, Wyble BP. A proposed function for hippocampal theta rhythm: separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation. 2002;14:793–817. [PubMed]
48. Givens B. Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport. 1996;8:159–163. [PubMed]
49. Tesche CD, Karhu J. Theta oscillations index human hippocampal activation during a working memory task. Proceedings of the National Academy of Sciences of the United States of America. 2000;97:919–924. [PMC free article] [PubMed]
••50. Rajkai C, Lakatos P, Chen C-M, Pincze Z, Karmos G, Schroeder CE. Transient Cortical Excitation at the Onset of Visual Fixation. Cerebral Cortex. 2008;18:200–209. Here, recordings from visual cortex as monkeys made saccades in the dark revealed that a transient excitatory response seen in the current source density (CSD), triggered by fixation onset, can be explained in part by an increase in phase concentration in the range of 3–8 Hz. In other words, because oscillatory phase after fixation onset is more uniform with respect to time after fixation than that before fixation onset due to a “phase resetting” mechanism, there is a net excitatory effect seen in the response-averaged activity. Furthermore, the amplitude of neural responses to visual stimuli was determined by the oscillatory phase at stimulus onset: stimuli that were flashed at an “ideal phase” of the CSD oscillation evoked higher-amplitude responses in the CSD as well as in neuronal spiking activity than stimuli that were flashed at different phases. [PubMed]
51. Lakatos P, Chen C-M, O’Connell MN, Mills A, Schroeder CE. Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex. Neuron. 2007;53:279–292. [PMC free article] [PubMed]
52. Melloni L, Schwiedrzik CM, Rodriguez E, Singer W. (Micro)Saccades, corollary activity and cortical oscillations. Trends in Cognitive Sciences. 2009;13:239–245. [PubMed]
53. Huerta PT, Lisman JE. Bidirectional synaptic plasticity induced by a single burst during cholinergic theta oscillation in CA1 in vitro. Neuron. 1995;15:1053–1063. [PubMed]
54. Hyman JM, Wyble BP, Goyal V, Rossi CA, Hasselmo ME. Stimulation in hippocampal region CA1 in behaving rats yields long-term potentiation when delivered to the peak of theta and long-term depression when delivered to the trough. Journal of Neuroscience. 2003;23:11725–11731. [PubMed]
55. McCartney H, Johnson AD, Weil ZM, Givens B. Theta reset produces optimal conditions for long-term potentiation. Hippocampus. 2004;14:684–687. [PubMed]
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

  • MedGen
    MedGen
    Related information in MedGen
  • PubMed
    PubMed
    PubMed citations for these articles

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...