Dynamic θ Frequency Coordination within and between the Prefrontal Cortex-Hippocampus Circuit during Learning of a Spatial Avoidance Task

Dickson, Conor; Holmes, Gregory L.; Barry, Jeremy M.

doi:10.1523/eneuro.0414-21.2022

Cited by 3 publications

(3 citation statements)

References 70 publications

(122 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Padilla-Coreano et al (2019) found that oscillatory optogenetic stimulation of hippocampal terminals in the mPFC during an avoidance behavior task maximally increased avoidance when delivered at a frequency of 8 Hz rather than 2, 4, or 20 Hz. And interestingly, Dickson et al (2022) found that coherence in theta subfrequencies (in particular at ;6, 9, and 11 Hz) changed dynamically during the course of the avoidance response. Furthermore, Kjaerby et al (2016) found that the effectiveness of theta band communication could be modulated by neurotransmitters.…”

Section: Implications For Ptsdmentioning

confidence: 92%

“…We also note that our modeling results coincide with the results of recent studies showing that sub-bands within the theta band are critical for communication within and between the mPFC and limbic structures and that neurotransmitters can enhance or impair communication within these structures in theta sub-bands. For instance, studies suggest that the coherence between the hippocampus and the mPFC of theta frequencies near the upper end of the theta range is important for avoidance learning (Padilla-Coreano et al, 2019;Dickson et al, 2022). Padilla-Coreano et al (2019) found that oscillatory optogenetic stimulation of hippocampal terminals in the mPFC during an avoidance behavior task maximally increased avoidance when delivered at a frequency of 8 Hz rather than 2, 4, or 20 Hz.…”

Section: Implications For Ptsdmentioning

confidence: 99%

See 1 more Smart Citation

Emotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder

2022

View full text Add to dashboard Cite

REM sleep is important for the processing of emotional memories, including fear memories. Rhythmic interactions, especially in the theta band, between the medial prefrontal cortex (mPFC) and limbic structures are thought to play an important role, but the ways in which memory processing occurs at a mechanistic and circuits level are largely unknown. To investigate how rhythmic interactions lead to fear extinction during REM sleep, we used a biophysically based model that included the infralimbic cortex (IL), a part of the mPFC with a critical role in suppressing fear memories. Theta frequency (4–12 Hz) inputs to a given cell assembly in IL, representing an emotional memory, resulted in the strengthening of connections from the IL to the amygdala and the weakening of connections from the amygdala to the IL, resulting in the suppression of the activity of fear expression cells for the associated memory. Lower frequency (4 Hz) theta inputs effected these changes over a wider range of input strengths. In contrast, inputs at other frequencies were ineffective at causing these synaptic changes and did not suppress fear memories. Under post-traumatic stress disorder (PTSD) REM sleep conditions, rhythmic activity dissipated, and 4 Hz theta inputs to IL were ineffective, but higher-frequency (10 Hz) theta inputs to IL induced changes similar to those seen with 4 Hz inputs under normal REM sleep conditions, resulting in the suppression of fear expression cells. These results suggest why PTSD patients may repeatedly experience the same emotionally charged dreams and suggest potential neuromodulatory therapies for the amelioration of PTSD symptoms.SIGNIFICANCE STATEMENTRhythmic interactions in the theta band between the mPFC and limbic structures are thought to play an important role in processing emotional memories, including fear memories, during REM sleep. The infralimbic cortex (IL) in the mPFC is thought to play a critical role in suppressing fear memories. We show that theta inputs to the IL, unlike other frequency inputs, are effective in producing synaptic changes that suppress the activity of fear expression cells associated with a given memory. Under PTSD REM sleep conditions, lower-frequency (4 Hz) theta inputs to the IL do not suppress the activity of fear expression cells associated with the given memory but, surprisingly, 10 Hz inputs do. These results suggest potential neuromodulatory therapies for PTSD.

show abstract

Section: Implications For Ptsdmentioning

confidence: 92%

Section: Implications For Ptsdmentioning

confidence: 99%

Emotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder

2022

View full text Add to dashboard Cite

show abstract

“…A growing body of evidence suggests that information sharing between the HPC and mPFC is required for cognitive processes and successful execution of behaviours (Harris and Gordon, 2015;Negrón-Oyarzo et al, 2018;Preston and Eichenbaum, 2013;Salimi et al, 2021;Tang et al, 2021;Wirt and Hyman, 2017). Recent evidence further highlights the importance of communication between the HPC and mPFC during learning and memory processes (Dickson et al, 2022;Morici et al, 2022). Efforts to understand the pathophysiology of various disorders have focused on identifying abnormalities in regions of the HPC and mPFC underlying symptoms of these disorders.…”

Section: Introductionmentioning

confidence: 99%

The role of aberrant neural oscillations in the hippocampal-medial prefrontal cortex circuit in neurodevelopmental and neurological disorders

Shing

Walker

Chang

2022

Neurobiology of Learning and Memory

View full text Add to dashboard Cite

Brain-Wide Projections and Differential Encoding of Prefrontal Neuronal Classes Underlying Learned and Innate Threat Avoidance

Gongwer¹,

Klune²,

Couto³

et al. 2023

J. Neurosci.

View full text Add to dashboard Cite

To understand how the brain produces behavior, we must elucidate the relationships between neuronal connectivity and function. The medial prefrontal cortex (mPFC) is critical for complex functions including decision-making and mood. mPFC projection neurons collateralize extensively, but the relationships between mPFC neuronal activity and brain-wide connectivity are poorly understood. We performed whole-brain connectivity mapping and fiber photometry to better understand the mPFC circuits that control threat avoidance in male and female mice. Using tissue clearing and light sheet fluorescence microscopy, we mapped the brain-wide axon collaterals of populations of mPFC neurons that project to nucleus accumbens (NAc), ventral tegmental area (VTA), or contralateral mPFC (cmPFC). We present DeepTraCE, for quantifying bulk-labeled axonal projections in images of cleared tissue, and DeepCOUNT, for quantifying cell bodies. Anatomical maps produced with DeepTraCE aligned with known axonal projection patterns and revealed class-specific topographic projections within regions. Using TRAP2 mice and DeepCOUNT, we analyzed whole-brain functional connectivity underlying threat avoidance. PL was the most highly connected node with functional connections to subsets of PL-cPL, PL-NAc and PL-VTA target sites. Using fiber photometry, we found that during threat avoidance, cmPFC and NAc-projectors encoded conditioned stimuli, but only when action was required to avoid threats. mPFC-VTA neurons encoded learned but not innate avoidance behaviors. Together our results present new and optimized approaches for quantitative whole-brain analysis and indicate that anatomically-defined classes of mPFC neurons have specialized roles in threat avoidance.SIGNIFICANCE STATEMENT:Understanding how the brain produces complex behaviors requires detailed knowledge of the relationships between neuronal connectivity and function. The medial prefrontal cortex (mPFC) plays a key role in learning, mood, and decision-making, including evaluating and responding to threats. mPFC dysfunction is strongly linked to fear, anxiety and mood disorders. Although mPFC circuits are clear therapeutic targets, gaps in our understanding of how they produce cognitive and emotional behaviors prevent us from designing effective interventions. To address this, we developed a high-throughput analysis pipeline for quantifying bulk-labeled fluorescent axons (DeepTraCE) or cell bodies (DeepCOUNT) in intact cleared brains. Using DeepTraCE, DeepCOUNT, and fiber photometry, we performed detailed anatomical and functional mapping of mPFC neuronal classes, identifying specialized roles in threat avoidance.

show abstract

Dynamic θ Frequency Coordination within and between the Prefrontal Cortex-Hippocampus Circuit during Learning of a Spatial Avoidance Task

Cited by 3 publications

References 70 publications

Emotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder

Emotional Memory Processing during REM Sleep with Implications for Post-Traumatic Stress Disorder

The role of aberrant neural oscillations in the hippocampal-medial prefrontal cortex circuit in neurodevelopmental and neurological disorders

Brain-Wide Projections and Differential Encoding of Prefrontal Neuronal Classes Underlying Learned and Innate Threat Avoidance

Contact Info

Product

Resources

About