Enhancing Prefrontal Neuron Activity Enables Associative Learning of Temporally Disparate Events

Volle, Julien; Yu, Xiaotian; Sun, Hanjie; Tanninen, Stephanie E.; Insel, Nathan; Takehara‐Nishiuchi, Kaori

doi:10.1016/j.celrep.2016.05.021

Cited by 21 publications

(31 citation statements)

References 49 publications

(57 reference statements)

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“…Among the 19 rats included in the behavioral analysis, 10 rats were used for the analysis of c-Fos expression. In addition to the 24 rats that were purchased for this study, we reanalyzed c-Fos expression data collected from 15 rats in our previous study (Volle et al, 2016). All procedures were in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals (Publication No.…”

Section: Methodsmentioning

confidence: 99%

“…All analyses were performed using custom code written in MATLAB (MathWorks) with the same procedure as that used in our previous studies (Volle et al, 2016; Morrissey et al, 2017). For each session per animal, the amplitude of the EMG signal during each 1 ms of time was calculated by subtracting the minimum signal from the maximum signal during that 1 ms window.…”

Section: Methodsmentioning

confidence: 99%

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Prefrontal Theta Oscillations Promote Selective Encoding of Behaviorally Relevant Events

Jarovi¹,

Volle²,

Yu³

et al. 2018

eNeuro

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The ability to capture the most relevant information from everyday experiences without constantly learning unimportant details is vital to survival and mental health. While decreased activity of the medial prefrontal cortex (mPFC) is associated with failed or inflexible encoding of relevant events in the hippocampus, mechanisms used by the mPFC to discern behavioral relevance of events are not clear. To address this question, we chemogenetically activated excitatory neurons in the mPFC of male rats and examined its impact on local network activity and differential associative learning dependent on the hippocampus. Rats were exposed to two neutral stimuli in two environments whose contingency with an aversive stimulus changed systematically across days. Over 2 weeks of differential and reversal learning, theta band activity began to ramp up toward the expected onset of the aversive stimulus, and this ramping activity tracked the subsequent shift of the set (stimulus modality to environment) predictive of the aversive stimulus. With chemogenetic mPFC activation, the ramping activity emerged within a few sessions of differential learning, which paralleled faster learning and stronger correlations between the ramping activity and conditioned responses. Chemogenetic mPFC activity, however, did not affect the adjustment of ramping activity or behavior during reversal learning or set-shifting, suggesting that the faster learning was not because of a general enhancement of attention, sensory, or motor processing. Thus, the dynamics of the mPFC network activation during events provide a relevance-signaling mechanism through which the mPFC exerts executive control over the encoding of those events in the hippocampus.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Prefrontal Theta Oscillations Promote Selective Encoding of Behaviorally Relevant Events

Jarovi¹,

Volle²,

Yu³

et al. 2018

eNeuro

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“…In fact, one hour after training in contextual fear conditioning, the transcription of multiple plasticity-related genes is upregulated in the mPFC, leading to immediate changes in synaptic structure and physiology (Bero et al, 2014). Parallel studies also showed that by enhancing the activity of mPFC neurons during training, it is possible to facilitate the acquisition of hippocampusdependent memories (Benn et al, 2016;Volle et al, 2016;Jarovi et al, 2018;Shibano et al, 2020). These observations, along with earlier findings of impaired hippocampus-dependent memories with disrupted mPFC (Hannesson et al, 2004;Takehara-Nishiuchi et al, 2005;Zhao et al, 2005;Barker and Warburton, 2008;Gilmartin and Helmstetter, 2010;Devito and Eichenbaum, 2011;Gilmartin et al, 2013;Bero et al, 2014), led us to hypothesize that the mPFC may work with, but not follows, the hippocampus to form new memories (Takehara-Nishiuchi, 2020b).…”

Section: Introductionmentioning

confidence: 99%

Prefrontal neural ensembles develop selective code for stimulus associations within minutes of novel experiences

Takehara‐Nishiuchi

Morrissey

Pilkiw

2020

Preprint

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Prevailing theories posit that the hippocampus rapidly learns stimulus conjunctions during novel experiences, whereas the neocortex learns slowly through subsequent, off-line interaction with the hippocampus. Parallel evidence, however, shows that the medial prefrontal cortex (mPFC, a critical node of the neocortical network supporting long-term memory storage) undergoes rapid modifications of gene expression, synaptic structure, and physiology at the time of encoding. These observations, along with impaired learning with disrupted mPFC, suggest that mPFC neurons may exhibit rapid neural plasticity during novel experiences; however, direct empirical evidence is lacking. We extracellularly recorded action potentials of cells in the prelimbic region of the mPFC, while male rats received a sequence of stimulus presentations for the first time in life. Moment-to-moment tracking of neural ensemble firing patterns revealed that the prelimbic network activity exhibited an abrupt transition within a minute after the first encounter of an aversive but not neutral stimulus. This network-level change was driven by ~15% of neurons that immediately elevated their spontaneous firing rates and developed firing responses to a neutral stimulus preceding the aversive stimulus within a few instances of their pairings. When a new sensory stimulus was paired with the same aversive stimulus, about half of these neurons generalized firing responses to the new stimulus association. Thus, prelimbic neurons are capable of rapidly forming ensemble codes for novel stimulus associations within minutes. This circuit property may enable the mPFC to rapidly detect and selectively encode the central content of novel experiences.

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“…In contrast, numerous studies have shown in various animal models that higher neuronal activity at the time of learning facilitates memory formation (Saar et al, 1998; Stackman et al, 2002; Zelcer et al, 2006; Han et al, 2009; Santini and Porter, 2010; Santini et al, 2012; Volle et al, 2016). This discrepancy may in part be because LTM formation in this paradigm is induced by inhibitory inputs, elicited by the conditioning stimuli, to the RPeD1.…”

Section: Discussionmentioning

confidence: 99%

Inverse Relationship between Basal Pacemaker Neuron Activity and Aversive Long-Term Memory Formation in Lymnaea stagnalis

Dong

Feng

2017

Front. Cell. Neurosci.

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Learning and memory formation are essential physiological functions. While quiescent neurons have long been the focus of investigations into the mechanisms of memory formation, there is increasing evidence that spontaneously active neurons also play key roles in this process and possess distinct rules of activity-dependent plasticity. In this study, we used a well-defined aversive learning model of aerial respiration in the mollusk Lymnaea stagnalis (L. stagnalis) to study the role of basal firing activity of the respiratory pacemaker neuron Right Pedal Dorsal 1 (RPeD1) as a determinant of aversive long-term memory (LTM) formation. We investigated the relationship between basal aerial respiration behavior and RPeD1 firing activity, and examined aversive LTM formation and neuronal plasticity in animals exhibiting different basal aerial respiration behavior. We report that animals with higher basal aerial respiration behavior exhibited early responses to operant conditioning and better aversive LTM formation. Early behavioral response to the conditioning procedure was associated with biphasic enhancements in the membrane potential, spontaneous firing activity and gain of firing response, with an early phase spanning the first 2 h after conditioning and a late phase that is observed at 24 h. Taken together, we provide the first evidence suggesting that lower neuronal activity at the time of learning may be correlated with better memory formation in spontaneously active neurons. Our findings provide new insights into the diversity of cellular rules of plasticity underlying memory formation.

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Enhancing Prefrontal Neuron Activity Enables Associative Learning of Temporally Disparate Events

Cited by 21 publications

References 49 publications

Prefrontal Theta Oscillations Promote Selective Encoding of Behaviorally Relevant Events

Prefrontal Theta Oscillations Promote Selective Encoding of Behaviorally Relevant Events

Prefrontal neural ensembles develop selective code for stimulus associations within minutes of novel experiences

Inverse Relationship between Basal Pacemaker Neuron Activity and Aversive Long-Term Memory Formation in Lymnaea stagnalis

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