Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats

Mitchell, SJ; Rawlins, J. N. P.; Steward, Oswald; Olton, David S.

doi:10.1523/jneurosci.02-03-00292.1982

Cited by 355 publications

(173 citation statements)

References 37 publications

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“…A representative histological example of a site of recording is shown in Figure 2A from an animal implanted with the hyper-drive. The recording from hippocampal area CA1 allowed us to characterize the patterns of theta-gamma phase amplitude observed before versus after the theta phase reversal in layer 2 MEC as shown in Figure 2, B and C (Mitchell and Ranck, 1980;Quilichini et al, 2010).…”

Section: Methodsmentioning

confidence: 99%

“…Notably, a theta phase reversal occurs around layer II (Mitchell and Ranck, 1980;Chrobak and Buzsáki, 1998) such that layer III is in-phase and layer I is out-of-phase with hippocampal area CA1 ). The theta-gamma coupling pattern of interest, as identified using the automatic selection approach described above, was observed on both sides of the phase reversal.…”

Section: Methodsmentioning

confidence: 99%

“…Theta is important for performance of memory and navigational tasks (Winson, 1978;Mitchell et al, 1982;Mizumori et al, 1990;Givens and Olton, 1994). Each phase of theta is characterized by distinct physiological dynamics.…”

Section: Introductionmentioning

confidence: 99%

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Cholinergic Blockade Reduces Theta-Gamma Phase Amplitude Coupling and Speed Modulation of Theta Frequency Consistent with Behavioral Effects on Encoding

et al. 2013

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Large-scale neural activation dynamics in the hippocampal-entorhinal circuit local field potential, observable as theta and gamma rhythms and coupling between these rhythms, is predictive of encoding success. Behavioral studies show that systemic administration of muscarinic acetylcholine receptor antagonists selectively impairs encoding, suggesting that they may also disrupt the coupling between the theta and gamma bands. Here, we tested the hypothesis that muscarinic antagonists selectively disrupt coupling between theta and gamma. Specifically, we characterized the effects of systemically administered scopolamine on movement-induced theta and gamma rhythms recorded in the superficial layers of the medial entorhinal cortex (MEC) of freely moving rats. We report the novel result that gamma power at the peak of theta was most reduced following muscarinic blockade, significantly shifting the phase of maximal gamma power to occur at later phases of theta. We also characterize the existence of multiple distinct gamma bands in the superficial layers of the MEC. Further, we observed that theta frequency was significantly less modulated by movement speed following muscarinic blockade. Finally, the slope relating speed to theta frequency, a correlate of familiarity with a testing enclosure, increased significantly less between the preinjection and recovery trials when scopolamine was administered during the intervening injection session than when saline was administered, suggesting that scopolamine reduced encoding of the testing enclosure. These data are consistent with computational models suggesting that encoding and retrieval occur during the peak and trough of theta, respectively, and support the theory that acetylcholine regulates the balance between encoding versus retrieval.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Cholinergic Blockade Reduces Theta-Gamma Phase Amplitude Coupling and Speed Modulation of Theta Frequency Consistent with Behavioral Effects on Encoding

et al. 2013

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“…Theta rhythm oscillations have also been shown extensively in the entorhinal cortex with both field potential and unit recording (Mitchell and Ranck 1980;Mitchell et al 1982;Alonso and Garcia-Austt 1987a,b;Stewart et al 1992;Quirk et al 1992). Theta rhythmic firing in entorhinal cortex may partly result from contributions of intrinsic membrane potential oscillations (Acker et al 2003;Fransén et al 2004;Giocomo et al 2007) or theta rhythmic properties of persistent spiking activity (Tahvildari et al 2007).…”

Section: Simulation Of Interfering Oscillatory Activitymentioning

confidence: 96%

Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function

Hasselmo

2007

Learning & Memory

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Many memory models focus on encoding of sequences by excitatory recurrent synapses in region CA3 of the hippocampus. However, data and modeling suggest an alternate mechanism for encoding of sequences in which interference between theta frequency oscillations encodes the position within a sequence based on spatial arc length or time. Arc length can be coded by an oscillatory interference model that accounts for many features of the context-dependent firing properties of hippocampal neurons observed during performance of spatial memory tasks. In continuous spatial alternation, many neurons fire selectively depending on the direction of prior or future response (left or right). In contrast, in delayed non-match to position, most neurons fire selectively for task phase (sample vs. choice), with less selectivity for left versus right. These seemingly disparate results are effectively simulated by the same model, based on mechanisms similar to a model of grid cell firing in entorhinal cortex. The model also simulates forward shifting of firing over trials. Adding effects of persistent firing with reset at reward locations addresses changes in context-dependent firing with different task designs. Arc length coding could contribute to episodic encoding of trajectories as sequences of states and actions.Many models of the hippocampus focus on strengthening of synaptic connections between neurons to encode associations between sequential patterns of neural activity representing items or locations (McNaughton and

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“…In the rat, theta oscillations always accompany voluntary movement and active exploration 2,5 . Theta oscillations are essential for the normal functioning of the hippocampus, because manipulations that disrupt them produce behavioural impairments that mimic hippocampal lesions 6,7 . The importance of theta oscillations is underscored by the fact that they reflect subthreshold membrane potentials [8][9][10] and strongly modulate the spiking 5,11,12,13 of hippocampal neurons.…”

mentioning

confidence: 99%

Hippocampal theta oscillations are travelling waves

Lubenov

Siapas

2009

Nature

440

422

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Theta oscillations clock hippocampal activity during awake behaviour and rapid eye movement (REM) sleep. These oscillations are prominent in the local field potential, and they also reflect the subthreshold membrane potential and strongly modulate the spiking of hippocampal neurons. The prevailing view is that theta oscillations are synchronized throughout the hippocampus, despite the lack of conclusive experimental evidence. In contrast, here we show that in freely behaving rats, theta oscillations in area CA1 are travelling waves that propagate roughly along the septotemporal axis of the hippocampus. Furthermore, we find that spiking in the CA1 pyramidal cell layer is modulated in a consistent travelling wave pattern. Our results demonstrate that theta oscillations pattern hippocampal activity not only in time, but also across anatomical space. The presence of travelling waves indicates that the instantaneous output of the hippocampus is topographically organized and represents a segment, rather than a point, of physical space.Theta oscillations are a prominent 4-10-Hz rhythm in the hippocampal local field potential (LFP) of all mammals studied to date 1-3 , including humans 4 . During wakefulness they are associated with different speciesspecific behaviours, and they are invariably present during REM sleep 2,3 . In the rat, theta oscillations always accompany voluntary movement and active exploration 2,5 . Theta oscillations are essential for the normal functioning of the hippocampus, because manipulations that disrupt them produce behavioural impairments that mimic hippocampal lesions 6,7 . The importance of theta oscillations is underscored by the fact that they reflect subthreshold membrane potentials [8][9][10] and strongly modulate the spiking 5,11,12,13 of hippocampal neurons. Furthermore, theta oscillations gate synaptic plasticity, because the timing of stimulation with respect to the phase of theta is important in determining the magnitude and direction of synaptic change 14,15 . Theta oscillations therefore offer macroscopic access to the internal clock of the hippocampal circuit, responsible for temporally patterning its operation. Such clocking is essential for the temporal coding of spatial information by place cells 5,16 , as evidenced by theta phase precession [17][18][19] . In addition to coding position, theta phase precession ensures that the order of place-cell firing over behavioural timescales (seconds) is preserved and compressed within individual theta cycles and inside the window of plasticity 18 . In the presence of spike-timing-dependent plasticity 20 , the resulting compression of temporal sequences offers a mechanism for the formation of hippocampal memory traces 21 . Furthermore, theta oscillations modulate activity not only in the hippocampus, but also in several subcortical, limbic and cortical structures [22][23][24] .If theta oscillations can be thought of as a clock, what time is it in different parts of the hippocampus? In other words, how does the phase of theta oscillation...

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Medial septal area lesions disrupt theta rhythm and cholinergic staining in medial entorhinal cortex and produce impaired radial arm maze behavior in rats

Cited by 355 publications

References 37 publications

Cholinergic Blockade Reduces Theta-Gamma Phase Amplitude Coupling and Speed Modulation of Theta Frequency Consistent with Behavioral Effects on Encoding

Cholinergic Blockade Reduces Theta-Gamma Phase Amplitude Coupling and Speed Modulation of Theta Frequency Consistent with Behavioral Effects on Encoding

Arc length coding by interference of theta frequency oscillations may underlie context-dependent hippocampal unit data and episodic memory function

Hippocampal theta oscillations are travelling waves

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