Prefrontal cortex neuronal ensembles encoding fear drive fear expression during long-term memory retrieval

Giannotti, Giuseppe; Heinsbroek, Jasper A.; Yue, Alexander J.; Deisseroth, Karl; Peters, Jamie

doi:10.1038/s41598-019-47095-7

Cited by 24 publications

(19 citation statements)

References 35 publications

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“…In fact, female mice had stronger relationships between ensemble reactivation and sucrose seeking in both the same and different contexts, although the number of significant relationships may have been limited by sample sizes in each sex. A similar phenomenon has been reported in fear conditioning: inhibition of a PrL ensemble recruited during fear conditioning reduced conditioned suppression of food seeking in females, but not males (Giannotti et al, 2019).…”

Section: Discussionsupporting

confidence: 68%

Comparison of prefrontal cortex sucrose seeking ensembles engaged in multiple seeking sessions: Context is key

Jessen

Bennett

Liu

et al. 2022

J of Neuroscience Research

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Encoding of memories, including those associated with prior drug or reward, is thought to take place within distinct populations of neurons, termed ensembles. Neuronal ensembles for drug‐ and reward‐seeking have been identified in regions of the medial prefrontal cortex, but much of our understanding of these ensembles is based on experiments that take place in a single reward‐associated environment and measure ensemble encoding over short durations of time. In contrast, reward seeking behavior is evident across different reward‐associated environments and persists over time. Using TetTag mice and Fos immunohistochemistry, we examined the relationship between persistent sucrose‐seeking and ensemble encoding in mice that undergo seeking sessions in the same or different sucrose self‐administration contexts 2 weeks apart. We found that prelimbic (PrL) and anterior cingulate cortex ensembles tagged in the first seeking session were highly sensitive to the context in which a second seeking session took place: reactivation of these ensembles was reduced in the same context but elevated in a distinct sucrose self‐administration context. Correlational analyses revealed that ensemble reactivation in the PrL was proportional to the persistence of sucrose seeking behavior across sessions in differing ways in female mice. In the same context, reactivation was proportional to the persistence of non‐reinforced operant responses, whereas in a distinct context, reactivation was proportional to the persistence of non‐reinforced head entries into the sucrose receptacle. This study underlines the importance of the medial prefrontal cortex importance in maintaining a reward‐seeking ensemble over time and identifies context‐dependent changes in behavioral correlates of ensemble reactivation.

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Section: Discussionsupporting

confidence: 68%

Comparison of prefrontal cortex sucrose seeking ensembles engaged in multiple seeking sessions: Context is key

Jessen

Bennett

Liu

et al. 2022

J of Neuroscience Research

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“…Previous studies have demonstrated that the mPFC projects to several limbic areas (e.g., amygdala, hippocampus, hypothalamus, and BNST) that modulate emotional responses ( Gabbott et al, 2005 ; Cerqueira et al, 2008 ; Kim and Cho, 2017 ; Ko, 2017 ; Giannotti et al, 2019 ). In addition, there is dense intracortical connectivity, indicating subregion integration ( McKlveen et al, 2019 ).…”

Section: Discussionmentioning

confidence: 99%

Glutamatergic Neurotransmission Controls the Functional Lateralization of the mPFC in the Modulation of Anxiety Induced by Social Defeat Stress in Male Mice

Santos-Costa

Baptista-de-Souza

Canto-de-Souza

et al. 2021

Front. Behav. Neurosci.

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The rodent medial prefrontal cortex (mPFC) is anatomically divided into cingulate (Cg1), prelimbic (PrL), and infralimbic (IL) subareas. The left and right mPFC (L and RmPFC) process emotional responses induced by stress-related stimuli, and LmPFC and RmPFC inhibition elicit anxiogenesis and anxiolysis, respectively. Here we sought to investigate (i) the mPFC functional laterality on social avoidance/anxiogenic-like behaviors in male mice subjected to chronic social defeat stress (SDS), (ii) the effects of left prelimbic (PrL) inhibition (with local injection of CoCl2) on the RmPFC glutamatergic neuronal activation pattern (immunofluorescence assay), and (iii) the effects of the dorsal right mPFC (Cg1 + PrL) NMDA receptor blockade (with local injection of AP7) on the anxiety induced by left dorsal mPFC inhibition in mice exposed to the elevated plus maze (EPM). Results showed that chronic SDS induced anxiogenic-like behaviors followed by the rise of ΔFosB labeling and by ΔFosB + CaMKII double-labeling bilaterally in the Cg1 and IL subareas of the mPFC. Chronic SDS also increased ΔFosB and by ΔFosB + CaMKII labeling only on the right PrL. Also, the left PrL inhibition increased cFos + CaMKII labeling in the contralateral PrL and IL. Moreover, anxiogenesis induced by the left PrL inhibition was blocked by NMDA receptor antagonist AP7 injected into the right PrL. These findings suggest the lateralized control of the glutamatergic neurotransmission in the modulation of emotional-like responses in mice subjected to chronic SDS.

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“…Shipman and colleagues demonstrated that inducible inactivation of the PL impairs the retrieval of action-outcome memories following brief but not extended training 39 . PL neurons may thus form an "early" memory engram for outcome-related information as animals gain initial experience with a task, as has been reported in fear conditioning contexts 40 . Meanwhile, the BLA represents specific outcome information that is motivationally significant and necessary for choosing between options 23 .…”

Section: Flexible Action Requires Blapl Connectionsmentioning

confidence: 76%

Cell adhesion factors during adolescence support amygdalo-cortical connections and flexible action later in life

Kietzman

Shapiro

Trinoskey-Rice

et al. 2021

Preprint

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Adolescent brain development is characterized by dramatic neuronal remodeling in the prefrontal cortex. This plasticity is presumed to act in part to “set the stage” for prefrontal cortical function in adulthood, but causal relationships have largely not been verified. Integrins are cell adhesion factors that provide a link between the extracellular matrix and the intracellular actin cytoskeleton. We find that β1-integrin presence in the prelimbic subregion of the prefrontal cortex (PL) during adolescence, but not adulthood, is necessary for adult mice to select actions based on reward likelihood and value. These behaviors require coordinated limbic-frontal-striatal circuits. We identified projections from the basolateral amygdala (BLA) to PL as being necessary for mice to express learned response strategies. We then visualized adolescent PL neurons receiving input from the BLA and projecting to the dorsomedial striatum (DMS), a primary striatal output by which the PL controls reward-related behavior. These projection-defined neurons had a more “adult-like” morphology relative to a general population of layer V PL neurons. β1-integrin loss caused the overexpression of stubby-type dendritic spines at the expense of more mature spines, a phenotype not observed when β1-integrins were silenced before or after adolescence. Together, these experiments localize β1-integrin-mediated cell adhesion activity within a developing di-synaptic circuit that coordinates flexible action.

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Prefrontal cortex neuronal ensembles encoding fear drive fear expression during long-term memory retrieval

Cited by 24 publications

References 35 publications

Comparison of prefrontal cortex sucrose seeking ensembles engaged in multiple seeking sessions: Context is key

Comparison of prefrontal cortex sucrose seeking ensembles engaged in multiple seeking sessions: Context is key

Glutamatergic Neurotransmission Controls the Functional Lateralization of the mPFC in the Modulation of Anxiety Induced by Social Defeat Stress in Male Mice

Cell adhesion factors during adolescence support amygdalo-cortical connections and flexible action later in life

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