Chronic stress disrupts neural coherence between cortico-limbic structures

Oliveira, João Filipe; Dias, Nuno; Correia, Mariana Lopes; Gama-Pereira, Filipa; Sardinha, Vanessa Morais; Lima, Ana; Oliveira, Ana F.; Jacinto, Luis; Ferreira, Daniela; Silva, Ana Maria; Reis, Joana; Cerqueira, João José; Sousa, Nuno

doi:10.3389/fncir.2013.00010

Cited by 48 publications

(68 citation statements)

References 44 publications

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“…This is indicative that the hyperactivation of vHPC and BLA was maintained over the course of the 3 weeks in stressed animals. Overactivation of vHPC and BLA by stress has been previously described in works on brain slices (Rainnie et al, 2004; Maggio and Segal, 2009) and anaesthetized rats (Kavushansky and Richter-Levin, 2006) including in the theta range (Oliveira et al, 2013) and appears to be in accordance with the dendritic hypertrophy observed in neurons of these brain regions after chronic stress exposure (Mitra et al, 2005), as a result of persistent hypercortisolism. Persistent hyperactivation of the amygdala with concurrent loss of inhibitory drive of the dHPC and the mPFC is also tied with the maladaptation of chronic stress through the contribution to the persistent overactivation of the HPA axis (Flandreau et al, 2012).…”

Section: Discussionsupporting

confidence: 66%

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Jacinto

Reis

Dias

et al. 2013

Front. Behav. Neurosci.

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Exposure to a novel environment triggers the response of several brain areas that regulate emotional behaviors. Here, we studied theta oscillations within the hippocampus (HPC)-amygdala (AMY)-medial prefrontal cortex (mPFC) network in exploration of a novel environment and subsequent familiarization through repeated exposures to that same environment; in addition, we assessed how concomitant stress exposure could disrupt this activity and impair both behavioral processes. Local field potentials (LFP) were simultaneously recorded from dorsal and ventral hippocampus (dHPC and vHPC, respectively), basolateral amygdala (BLA) and mPFC in freely behaving rats while they were exposed to a novel environment, then repeatedly re-exposed over the course of 3 weeks to that same environment and, finally, on re-exposure to a novel unfamiliar environment. A longitudinal analysis of theta activity within this circuit revealed a reduction of vHPC and BLA theta power and vHPC-BLA theta coherence through familiarization which was correlated with a return to normal exploratory behavior in control rats. In contrast, a persistent over-activation of the same brain regions was observed in stressed rats that displayed impairments in novel exploration and familiarization processes. Importantly, we show that stress also affected intra-hippocampal synchrony and heightened the coherence between vHPC and BLA. In summary, we demonstrate that modulatory theta activity in the aforementioned circuit, namely in the vHPC and BLA, is correlated with the expression of anxiety in novelty-induced exploration and familiarization in both normal and pathological conditions.

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Section: Discussionsupporting

confidence: 66%

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Jacinto

Reis

Dias

et al. 2013

Front. Behav. Neurosci.

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“…4) in MGPNS rats, relative to controls. These findings are in sharp contrast with a study of brain signals recorded under anesthesia from rats chronically stressed during adulthood (Oliveira et al, 2013). These authors report increased power spectrum density (4-40 Hz range) in the vHPC and mPFC, but decreased coherence between these structures.…”

Section: Discussioncontrasting

confidence: 59%

Multigenerational prenatal stress increases the coherence of brain signaling among cortico–striatal–limbic circuits in adult rats

et al. 2015

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“…Indeed, in rodent models of stress (Jacinto et al, 2013; Oliveira et al, 2013) and schizophrenia (Sigurdsson et al, 2010) coherences between VH and PFC are decreased. Likewise, the majority of studies in children with ASD have demonstrated reduced coherences (Coben et al, 2008; Khan et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

Alterations in sociability and functional brain connectivity caused by early-life seizures are prevented by bumetanide

Holmes¹,

Tian²,

Hernan³

et al. 2015

Neurobiology of Disease

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There is a well-described association between infantile epilepsy and pervasive cognitive and behavioral deficits, including a high incidence of autism spectrum disorders. Despite the robustness of the relationship between early-life seizures and the development of autism, the pathophysiological mechanism by which this occurs has not been explored. As a result of increasing evidence that autism is a disorder of brain connectivity we hypothesized that early-life seizures would interrupt normal brain connectivity during brain maturation and result in an autistic phenotype. Normal rat pups underwent recurrent flurothyl-induced seizures from postnatal (P) day 5-14 and then tested, along with controls, for developmental alterations of development brain oscillatory activity from P18-25. Specifically we wished to understand how normal changes in rhythmicity in and between brain regions change as a function of age and if this rhythmicity is altered or interrupted by early life seizures. In rat pups with early-life seizures, field recordings from dorsal and ventral hippocampus and prefrontal cortex demonstrated marked increase in coherence as well as a decrease in voltage correlation at all bandwidths compared to controls while there were minimal differences in total power and relative power spectral densities. Rats with early-life seizures had resulting impairment in the sociability and social novelty tests but demonstrated no evidence of increased activity or generalized anxiety as measured in the open field. In addition, rats with early-life seizures had lower seizure thresholds than controls, indicating long-standing alterations in the excitatory/inhibition balance. Bumetanide, a pharmacological agent that blocks the activity of NKCC1 and induces a significant shift of ECl toward more hyperpolarized values, administration at the time of the seizures precluded the subsequent abnormalities in coherence and voltage correlation and resulted in normal sociability and seizure threshold. Taken together these findings indicate that early-life seizures alter the development of oscillations and result in autistic-like behaviors. The altered communication between these brain regions could reflect the physiological underpinnings underlying social cognitive deficits seen in autism spectrum disorders.

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Chronic stress disrupts neural coherence between cortico-limbic structures

Cited by 48 publications

References 44 publications

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Stress affects theta activity in limbic networks and impairs novelty-induced exploration and familiarization

Multigenerational prenatal stress increases the coherence of brain signaling among cortico–striatal–limbic circuits in adult rats

Alterations in sociability and functional brain connectivity caused by early-life seizures are prevented by bumetanide

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