Cholinergic modulation of the CAN current may adjust neural dynamics for active memory maintenance, spatial navigation and time-compressed replay

Yoshida, Masatoshi; Knauer, Beate; Jochems, Arthur

doi:10.3389/fncir.2012.00010

Cited by 26 publications

(30 citation statements)

References 148 publications

(256 reference statements)

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“…This could contribute to the impairment of encoding of episodic memories caused by muscarinic cholinergic antagonists such as scopolamine [76;77]. In addition, this cholinergic modulation of the persistent firing property might support switching between encoding and consolidation functions of the MTL [16;63]. …”

Section: Discussionmentioning

confidence: 99%

“…Active maintenance of memory may help association of temporally separated information which is thought to be necessary for the formation of long-term episodic and sequential memory [11–13]. In vivo recordings in animals [14–16] and fMRI in humans [14;15] have revealed persistent activity during the trace or delay period of memory tasks when information retention is necessary (reviewed in [16]). These indicate that persistent neural firing may support temporal association by providing a means to retain necessary information across the temporal gap.…”

Section: Introductionmentioning

confidence: 99%

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Cholinergic receptor activation supports persistent firing in layer III neurons in the medial entorhinal cortex

Jochems

Reboreda

Hasselmo

et al. 2013

Behavioural Brain Research

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Medial temporal lobe (MTL) areas are crucial for memory tasks such as spatial working memory and temporal association memory, which require an active maintenance of memory for a short period of time (a few hundred milliseconds to tens of seconds). Recent work has shown that the projection from layer III neurons in the medial entorhinal cortex (MEC) to hippocampal region CA1, the temporoammonic (TA) pathway, might be specially important for these memory tasks. In addition, lesions to the entorhinal cortex disrupt persistent firing in CA1 which is believed to support active maintenance of memory. Injection of cholinergic antagonists and group I mGlu receptor antagonists to the MEC impairs spatial working memory and temporal association memory. Consistent with this, we have shown that group I mGlu receptor activation supports persistent firing in principal cells of the MEC layer III in vitro (Yoshida et al., 2008). However, it still remains unknown whether cholinergic receptor activation also supports persistent firing in MEC layer III neurons. In this paper, we tested this in MEC layer III cells using both ruptured and perforated whole-cell recordings in vitro. We report that the majority of cells we recorded from in MEC layer III show persistent firing during perfusion of the cholinergic agonist carbachol (2 – 10 μM). In addition, repeated stimulation gradually suppressed persistent firing. We further discuss the possible role of persistent firing in memory in general.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Cholinergic receptor activation supports persistent firing in layer III neurons in the medial entorhinal cortex

Jochems

Reboreda

Hasselmo

et al. 2013

Behavioural Brain Research

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“…Most recently, persistent firing was also detected in the hippocampus (HC) [19], [26], [27], which has long been recognized as important for normal trace conditioning [32], [34], [35]. In support of the persistent-firing hypothesis, trace but not delay, fear conditioning is profoundly impaired by infusions of mAChR antagonists into PR [30], EC [16], and HC [36].…”

Section: Introductionmentioning

confidence: 99%

Muscarinic Receptors in Amygdala Control Trace Fear Conditioning

2012

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Intelligent behavior requires transient memory, which entails the ability to retain information over short time periods. A newly-emerging hypothesis posits that endogenous persistent firing (EPF) is the neurophysiological foundation for aspects or types of transient memory. EPF is enabled by the activation of muscarinic acetylcholine receptors (mAChRs) and is triggered by suprathreshold stimulation. EPF occurs in several brain regions, including the lateral amygdala (LA). The present study examined the role of amygdalar mAChRs in trace fear conditioning, a paradigm that requires transient memory. If mAChR-dependent EPF selectively supports transient memory, then blocking amygdalar mAChRs should impair trace conditioning, while sparing delay and context conditioning, which presumably do not rely upon transient memory. To test the EPF hypothesis, LA was bilaterally infused, prior to trace or delay conditioning, with either a mAChR antagonist (scopolamine) or saline. Computerized video analysis quantified the amount of freezing elicited by the cue and by the training context. Scopolamine infusion profoundly reduced freezing in the trace conditioning group but had no significant effect on delay or context conditioning. This pattern of results was uniquely anticipated by the EPF hypothesis. The present findings are discussed in terms of a systems-level theory of how EPF in LA and several other brain regions might help support trace fear conditioning.

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“…These two protocols, along with additional control conditions (e.g., unpaired pseudo-random CS-US presentations), provide a powerful means to evaluate the contribution of different brain regions to temporal associative learning. For these reasons, in this review we focus discussion primarily on these behavioral paradigms, the functional dissections of the EC-HPC circuits and the physiological mechanisms that subserve temporal aspects of episodic memory, although there are reviews that discuss additional physiological mechanisms of temporal associative learning (Hasselmo and Stern 2006;Yoshida et al 2012;Eichenbaum 2014).…”

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confidence: 99%

Entorhinal–hippocampal neuronal circuits bridge temporally discontiguous events

2015

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The entorhinal cortex (EC) -hippocampal (HPC) network plays an essential role for episodic memory, which preserves spatial and temporal information about the occurrence of past events. Although there has been significant progress toward understanding the neural circuits underlying the spatial dimension of episodic memory, the relevant circuits subserving the temporal dimension are just beginning to be understood. In this review, we examine the evidence concerning the role of the EC in associating events separated by time-or temporal associative learning-with emphasis on the function of persistent activity in the medial entorhinal cortex layer III (MECIII) and their direct inputs into the CA1 region of HPC. We also discuss the unique role of Island cells in the medial entorhinal cortex layer II (MECII), which is a newly discovered direct feedforward inhibitory circuit to CA1. Finally, we relate the function of these entorhinal cortical circuits to recent findings concerning hippocampal time cells, which may collectively activate in sequence to bridge temporal gaps between discontiguous events in an episode.

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Cholinergic modulation of the CAN current may adjust neural dynamics for active memory maintenance, spatial navigation and time-compressed replay

Cited by 26 publications

References 148 publications

Cholinergic receptor activation supports persistent firing in layer III neurons in the medial entorhinal cortex

Cholinergic receptor activation supports persistent firing in layer III neurons in the medial entorhinal cortex

Muscarinic Receptors in Amygdala Control Trace Fear Conditioning

Entorhinal–hippocampal neuronal circuits bridge temporally discontiguous events

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