Phase matters: responding to and learning about peripheral stimuli depends on hippocampal θ phase at stimulus onset

Nokia, Miriam S.; Waselius, Tomi; Mikkonen, Jarno E.; Wikgren, Jan; Penttonen, Markku

doi:10.1101/lm.038166.115

Cited by 13 publications

(22 citation statements)

References 31 publications

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“…In fact, almost all (90%) of the animals in the diastole group reached a limit of 80% CRs per session, whereas only one-half the animals in the systole group and less than one-third of those in the random group reached this limit during the 14 sessions of trace eyeblink conditioning. The animals in the diastole group also learned exceptionally well compared with previous results from our laboratory using the same paradigm for trace eyeblink conditioning (Nokia and Wikgren 2014;Nokia et al 2015;Waselius et al 2018).…”

Section: Experiments 2: Rabbit Eyeblink Conditioning and Hippocampal Fsupporting

confidence: 58%

“…The critical role of the hippocampal theta activity in declarative learning is supported by a multitude of experimental findings (Berry and Seager 2001;Berry and Thompson 1978;Griffin et al 2004;Wikgren 2010, 2014; for conflicting findings, see Múnera et al 2001). Overall, temporally robust hippocampal thetaband responses to the conditioned stimulus predict good learning (Nokia et al 2015).…”

Section: Introductionmentioning

confidence: 99%

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Learning by heart: cardiac cycle reveals an effective time window for learning

Waselius

Wikgren

Halkola

et al. 2018

Journal of Neurophysiology

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Cardiac cycle phase is known to modulate processing of simple sensory information. This effect of the heartbeat on brain function is likely exerted via baroreceptors, the neurons sensitive for changes in blood pressure. From baroreceptors, the signal is conveyed all the way to the forebrain and the medial prefrontal cortex. In the two experiments reported, we examined whether learning, as a more complex form of cognition, can be modulated by the cardiac cycle phase. Human participants ( experiment 1) and rabbits ( experiment 2) were trained in trace eyeblink conditioning while neural activity was recorded. The conditioned stimulus was presented contingently with either the systolic or diastolic phase of the cycle. The tone used as the conditioned stimulus evoked amplified responses in both humans (electroencephalogram from "vertex," Cz) and rabbits (hippocampal CA1 local field potential) when its onset was timed at systole. In humans, the cardiac cycle phase did not affect learning, but rabbits trained at diastole learned significantly better than those trained at a random phase of the cardiac cycle. In summary, our results suggest that neural processing of external stimuli and also learning can be affected by targeting stimuli on the basis of cardiac cycle phase. These findings might be useful in applications aimed at maximizing or minimizing the effects of external stimulation. NEW & NOTEWORTHY It has been shown that rapid changes in bodily states modulate neural processing of external stimulus in brain. In this study, we show that modulation of neural processing of external stimulus and learning about it depends on the phase of the cardiac cycle. This is a novel finding that can be applied to optimize associative learning.

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Section: Experiments 2: Rabbit Eyeblink Conditioning and Hippocampal Fsupporting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

Learning by heart: cardiac cycle reveals an effective time window for learning

Waselius

Wikgren

Halkola

et al. 2018

Journal of Neurophysiology

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“…; Nokia et al . ). Further, according to Buzsaki's theory (Buzsáki, ), during a rest period following the initial learning event, CA3 neurons potentiated most recently initiate ripples, that is, induce firing of the larger ensemble of previously activated CA3 neurons and their target CA1 pyramidal cells.…”

Section: Discussionmentioning

confidence: 97%

“…According to Buzsáki's two-stage theory (Buzsáki, 1989), during epochs of theta, granule cells in the dentate gyrus encode incoming information about external events arriving from the entorhinal cortex into weak representations in the CA3. Interestingly, the phase of theta seems to modulate hippocampal responses to external stimuli and learning about those stimuli (Hasselmo et al 2002;Nokia et al 2015). Further, according to Buzsaki's theory (Buzsáki, 1989), during a rest period following the initial learning event, CA3 neurons potentiated most recently initiate ripples, that is, induce firing of the larger ensemble of previously activated CA3 neurons and their target CA1 pyramidal cells.…”

Section: Discussionmentioning

confidence: 99%

Hippocampal electrical stimulation disrupts associative learning when targeted at dentate spikes

Nokia

Gureviciene

Waselius

et al. 2017

The Journal of Physiology

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Key points Dentate spikes are fast fluctuations of hilar local‐field potentials that take place during rest and are thought to reflect input arriving from the entorhinal cortex to the hippocampus. During dentate spikes, neuronal firing in hippocampal input (dentate gyrus) and output (CA1/CA3) regions is uncoupled. To date, the behavioural significance of dentate spikes is unknown. Here, we provide evidence that disrupting the dentate spike‐related uncoupling of the dentate gyrus and the CA1/CA3 subregions for 1 h after training retards associative learning. We suggest dentate spikes play a significant role in memory consolidation. Abstract Hippocampal electrophysiological oscillations, namely theta and ripples, have been implicated in encoding and consolidation of new memories, respectively. According to existing literature, hippocampal dentate spikes are prominent, short‐duration (<30 ms), large‐amplitude (∼2–4 mV) fluctuations in hilar local‐field potentials that take place during awake immobility and sleep. Interestingly, previous studies indicate that during dentate spikes dentate gyrus granule cells increase their firing while firing of CA1 pyramidal cells are suppressed, thus resulting in momentary uncoupling of the two hippocampal subregions. To date, the behavioural significance of dentate spikes is unknown. Here, to study the possible role of dentate spikes in learning, we trained adult male Sprague–Dawley rats in trace eyeblink classical conditioning. For 1 h immediately following each conditioning session, one group of animals received hippocampal stimulation via the ventral hippocampal commissure (vHC) contingent on dentate spikes to disrupt the uncoupling between the dentate gyrus and the CA1 subregions. A yoked control group was stimulated during immobility, irrespective of brain state, and another control group was not stimulated at all. As a result, learning was impaired only in the group where vHC stimulation was administered contingent on dentate spikes. Our results suggest dentate spikes and/or the associated uncoupling of the dentate gyrus and the CA1 play a significant role in memory consolidation. Dentate spikes could possibly reflect reactivation and refinement of a memory trace within the dentate gyrus triggered by input from the entorhinal cortex.

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“…In fact, Berry et al reported that presenting trials when theta power is high results in faster learning of trace (or delay) EBC as compared with presenting trials when theta is not present (Cicchese, Darling, & Berry, ; Seager, Johnson, Chabot, Asaka, & Berry, ). Failures to replicate this effect may be due to presentation of the conditioning stimuli at a sub‐optimal phase of the theta cycle (Nokia, Waselius, Mikkonen, Wikgren, & Penttonen, ), hence an analysis of theta phase and phase resetting is important. Regardless, stimulus‐specific theta modulations in CA1 remain strong throughout acquisition and consolidated performance of trace eyeblink conditioning (Hattori, Chen, et al, ).…”

Section: Introductionmentioning

confidence: 99%

Differential responsivity of neurons in perirhinal cortex, lateral entorhinal cortex, and dentate gyrus during time‐bridging learning

2018

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Many studies have focused on the function of hippocampal region CA1 as a critical site for associative memory, but much less is known about changes in the afferents to CA1. Here we report the activity of multiple single neurons from perirhinal and entorhinal cortex and from dentate gyrus during trace eyeblink conditioning as well as consolidated recall, and in pseudo‐conditioned control rabbits. We also report an analysis of theta activity filtered from the local field potential (LFP). Our results show early associative changes in single‐neuron firing rate as well as theta oscillations in lateral entorhinal cortex (EC) and dentate gyrus (DG), and increases in the number of responsive neurons in perirhinal cortex. In both EC and DG, a subset of neurons from conditioned animals exhibited an elevated baseline firing rate and large responses to the conditioned stimulus and trace period. A similar population of cells has been seen in DG and in medial, but not lateral, EC during spatial tasks, suggesting that lateral EC contains cells responsive to a temporal associative task. In contrast to recent studies in our laboratory that found significant CA1 contributions to long‐term memory, the activity profiles of neurons within EC and DG were similar for conditioned and pseudoconditioned rabbits during post‐consolidation sessions. Collectively these results demonstrate that individual subregions of medial temporal lobe differentially support new and remotely acquired memories. Neuron firing profiles were similar on training trials when conditioned responses were and were not exhibited, demonstrating that these temporal lobe regions represent the CS–US association and do not control the behavioral response. The analysis of theta activity revealed that theta power was modulated by the conditioning stimuli in both the conditioned and pseudoconditioned groups and that although both groups exhibited a resetting of phase to the corneal airpuff, only the conditioned group exhibited a resetting of phase to the whisker conditioned stimulus.

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Phase matters: responding to and learning about peripheral stimuli depends on hippocampal θ phase at stimulus onset

Cited by 13 publications

References 31 publications

Learning by heart: cardiac cycle reveals an effective time window for learning

Learning by heart: cardiac cycle reveals an effective time window for learning

Hippocampal electrical stimulation disrupts associative learning when targeted at dentate spikes

Differential responsivity of neurons in perirhinal cortex, lateral entorhinal cortex, and dentate gyrus during time‐bridging learning

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