Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state

Huerta, Patricio T.; Lisman, John

doi:10.1038/364723a0

Cited by 519 publications

(344 citation statements)

References 26 publications

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“…Many studies have demonstrated that cholinergic modulation enhances long-term potentiation in cortical structures including hippocampus, neocortex and piriform cortex (Blitzer et al, 1990;Brocher et al, 1992;Huerta & Lisman, 1993;Patil et al, 1998). However, the experiment presented here addresses a separate issue.…”

Section: Relation To Other Physiological Datamentioning

confidence: 87%

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Linster

Maloney

Patil

et al. 2003

Neurobiology of Learning and Memory

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Computational modeling assists in analyzing the specific functional role of the cellular effects of acetylcholine within cortical structures. In particular, acetylcholine may regulate the dynamics of encoding and retrieval of information by regulating the magnitude of synaptic transmission at excitatory recurrent connections. Many abstract models of associative memory function ignore the influence of changes in synaptic strength during the storage process and apply the effect of these changes only during a socalled recall-phase. Efforts to ensure stable activity with more realistic, continuous updating of the synaptic strength during the storage process have shown that the memory capacity of a realistic cortical network can be greatly enhanced if cholinergic modulation blocks transmission at synaptic connections of the association fibers during the learning process. We here present experimental data from an olfactory cortex brain slice preparation showing that previously potentiated fibers show significantly greater suppression (presynaptic inhibition) by the cholinergic agonist carbachol than unpotentiated fibers. We conclude that low suppression of non-potentiated fibers during the learning process ensures the formation of self-organized representations in the neural network while the higher suppression of previously potentiated fibers minimizes interference between overlapping patterns. We show in a computational model of olfactory cortex, that, together, these two phenomena reduce the overlap between patterns that are stored within the same neural network structure. These results further demonstrate the contribution of acetylcholine to mechanisms of cortical plasticity. The results are consistent with the extensive evidence supporting a role for acetylcholine in encoding of new memories and enhancement of response to salient sensory stimuli.

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Section: Relation To Other Physiological Datamentioning

confidence: 87%

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Linster

Maloney

Patil

et al. 2003

Neurobiology of Learning and Memory

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“…Recently there has been much progress in understanding the role of theta oscillations in organizing neuronal activity in animals (O' Keefe & Dostrovsky, 1971;O'Keefe & Recce, 1993;Nádasdy et al, 1999;Huerta & Lisman, 1993;Montgomery et al, 2008). This knowledge resulted in functional theories implicating theta in memory and other cognitive processes.…”

Section: Introductionmentioning

confidence: 99%

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Clemens

Borbély

Weiss

et al. 2013

Neuroscience Research

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Hippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REM-dependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previous studies providing further indication that it is delta rather than theta that should be regarded as a human analogue of the animal RSA.NeuroscienceResearch, Volume 76, Issues 1-2, May-June 2013, Pages 67-75, DOI: 10.1016/j.neures.2013.03.004 HighlightsMesiotemporal EEG activity was assessed during a spatial task in epilepsy patients.Low frequency spectral power increased during all three navigation conditions.There was no change during task performance in the theta frequency band.Delta rather than theta should be regarded as a human analogue of animal theta. *Highlights (for review) Click here to download Highlights (for review): highlights.doc 2 AbstractHippocampal theta or rhythmic slow activity (RSA) occurring during exploratory behaviors and rapid-eye-movement (REM) sleep is a characteristic and well-identifiable oscillatory rhythm in animals. In contrast, controversy surrounds the existence and electrophysiological correlates of this activity in humans. Some argue that the human hippocampal theta occurs in short and phasic bursts. On the contrary, our earlier studies provide evidence that REMdependent mesiotemporal RSA is continuous like in animals but instead of the theta it falls in the delta frequency range. Here we used a virtual navigation task in 24 epilepsy patients implanted with foramen ovale electrodes. EEG was analyzed for 1-Hz wide frequency bins up to 10 Hz according to four conditions: resting, non-learning route-following, acquisition and recall. We found progressively increasing spectral power in frequency bins up the 4 Hz across these conditions. No spectral power increase relative to resting was revealed within the traditional theta band and above in any of the navigation conditions. Thus the affected frequency bins were below the theta band and were similar to those characterizing REM sleep in our previ...

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“…They have been suggested to set the temporal dynamics needed to organize synaptic plasticity and implement learning at the network level (Larson and Lynch, 1986;Huerta and Lisman, 1993;Hasselmo et al, 2002).…”

Section: Oscillatory Activitymentioning

confidence: 99%

Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits

2004

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ABSTRACT:It has been suggested that hippocampal mode shifting between a storage and a retrieval state might be under the control of acetylcholine (ACh) levels, as set by an autoregulatory hippocampo-septohippocampal loop. The present study investigates how such a mechanism might operate in a large-scale connectionist model of this circuitry that takes into account the major hippocampal subdivisions, oscillatory population dynamics and the time scale on which ACh exerts its effects in the hippocampus. The model assumes that hippocampal mode shifting is regulated by a novelty signal generated in the hippocampus. The simulations suggest that this signal originates in the dentate. Novel patterns presented to this structure lead to brief periods of depressed firing in the hippocampal circuitry. During these periods, an inhibitory influence of the hippocampus on the septum is lifted, leading to increased firing of cholinergic neurons. The resulting increase in ACh release in the hippocampus produces network dynamics that favor learning over retrieval. Resumption of activity in the hippocampus leads to the reinstatement of inhibition. Despite theta-locked rhythmic firing of ACh neurons in the septum, ACh modulation in the model fluctuates smoothly on a time scale of seconds. It is shown that this is compatible with the time scale on which memory processes take place. A number of strong predictions regarding memory function are derived from the model.

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Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state

Cited by 519 publications

References 26 publications

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Enhanced cholinergic suppression of previously strengthened synapses enables the formation of self-organized representations in olfactory cortex

Increased mesiotemporal delta activity characterizes virtual navigation in humans

Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits

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