The ventral hippocampus and the lateral septum work in tandem to regulate rats' open-arm exploration in the elevated plus-maze

Trent, Natalie L.; Menard, Janet L.

doi:10.1016/j.physbeh.2010.04.035

Cited by 63 publications

(53 citation statements)

References 65 publications

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“…Using rodent approach–avoidance conflict tests, such as the elevated plus maze (EPM) or open-field test (OFT), a plethora of lesion and drug infusion studies have implicated the ventral hippocampus and medial prefrontal cortex (mPFC) in the control of such behaviors (Gray and McNaughton, 2000; Kjelstrup et al, 2002; Trent and Menard, 2010; Weeden et al, 2015; Ito and Lee, 2016). In line with these findings, a recent lesion study suggested a similar role of the human homolog, the anterior hippocampus, in anxiety-like behavior (Bach et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

et al. 2017

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Neural oscillations in hippocampus and medial prefrontal cortex (mPFC) are a hallmark of rodent anxiety models that build on conflict between approach and avoidance. Yet, the function of these oscillations, and their expression in humans, remain elusive. Here, we used magnetoencephalography (MEG) to investigate neural oscillations in a task that simulated approach–avoidance conflict, wherein 23 male and female human participants collected monetary tokens under a threat of virtual predation. Probability of threat was signaled by color and learned beforehand by direct experience. Magnitude of threat corresponded to a possible monetary loss, signaled as a quantity. We focused our analyses on an a priori defined region-of-interest, the bilateral hippocampus. Oscillatory power under conflict was linearly predicted by threat probability in a location consistent with right mid-hippocampus. This pattern was specific to the hippocampus, most pronounced in the gamma band, and not explained by spatial movement or anxiety-like behavior. Gamma power was modulated by slower theta rhythms, and this theta modulation increased with threat probability. Furthermore, theta oscillations in the same location showed greater synchrony with mPFC theta with increased threat probability. Strikingly, these findings were not seen in relation to an increase in threat magnitude, which was explicitly signaled as a quantity and induced similar behavioral responses as learned threat probability. Thus, our findings suggest that the expression of hippocampal and mPFC oscillatory activity in the context of anxiety is specifically linked to threat memory. These findings resonate with neurocomputational accounts of the role played by hippocampal oscillations in memory.SIGNIFICANCE STATEMENT We use a biologically relevant approach–avoidance conflict test in humans while recording neural oscillations with magnetoencephalography to investigate the expression and function of hippocampal oscillations in human anxiety. Extending nonhuman studies, we can assign a possible function to hippocampal oscillations in this task, namely threat memory communication. This blends into recent attempts to elucidate the role of brain synchronization in defensive responses to threat.

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Section: Introductionmentioning

confidence: 99%

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

et al. 2017

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“…For example, social interaction is inherently stressful rodents (DeVries, 2002), and it reliably activates the PVN, a key stress-regulatory brain region (Sawchenko et al, 1996). Resident exposure also impacts the general level of arousal and anxiety, and activation of the LS has been implicated in these processes (Trent and Menard, 2010). Rats are also highly sensitive to olfactory cues, and intruder-elicited activation of Pir and MeA, both of which process olfactory stimuli (Gottfried, 2010; Price, 2003), likely represents strong olfactory stimulation by intruder presentation.…”

Section: Discussionmentioning

confidence: 99%

Pattern of forebrain activation in high novelty-seeking rats following aggressive encounter

Clinton¹,

Kerman²,

Orr³

et al. 2011

Brain Research

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We have previously demonstrated that selectively-bred High (bHR) and Low (bLR) novelty-seeking rats exhibit agonistic differences, with bHRs acting in a highly aggressive manner when facing homecage intrusion. In order to discover the specific neuronal pathways responsible for bHRs’ high levels of aggression, the present study compared c-fos mRNA expression in several forebrain regions of bHR/bLR males following this experience. bHR/bLR males were housed with female rats for two weeks, and then the females were replaced with a male intruder for 10 min. bHR/bLR residents were subsequently sacrificed by rapid decapitation, and their brains were removed and processed for c-fos in situ hybridization. Intrusion elicited robust c-fos mRNA expression in both phenotypes throughout the forebrain, including the septum, amygdala, hippocampus, cingulate cortex, and the hypothalamus. However, bHRs and bLRs exhibited distinct activation patterns in select areas. Compared to bHR rats, bLRs expressed greater c-fos in the lateral septum and within multiple hypothalamic nuclei, while bHRs showed greater activation in the arcuate hypothalamic nucleus and in the hippocampus. No bHR/bLR differences in c-fos expression were detected in the amygdala, cortical regions, and striatum. We also found divergent 5-HT1A receptor mRNA expression within some of these same areas, with bLRs having greater 5-HT1A, but not 5-HT1B, receptor mRNA levels in the septum, hippocampus and cingulate cortex. These findings, together with our earlier work, suggest that bHRs exhibit altered serotonergic functioning within select circuits during an aggressive encounter.

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“…Ipsilateral projections from vHPC to LS convey an anxiety signal; bilateral blockade of activity in either structure using muscimol increases open arm exploration in the EPM, as does disconnection of the two using pharmacological inactivation of vHPC in one hemisphere and concurrent inactivation of the contralateral LS 95 . Corticotropin releasing factor receptor (CRFR) activation in the LS increases anxiety-related phenotypes 96 by way of activation of CRFR type 2 expressing GABAergic projection neurons residing there 97 In addition to producing anxiety-like behaviors via projections to the LS, the vHPC supports the interpretation of a given situation as threatening through its reciprocal connection with the BLA as well as its efferent projections to the mPFC.…”

Section: Microcircuits and Interactions Among Nodesmentioning

confidence: 99%

Resolving the neural circuits of anxiety

2015

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Although anxiety disorders represent a major societal problem demanding new therapeutic targets, these efforts have languished in the absence of a mechanistic understanding of this subjective emotional state. While it is impossible to know with absolute certainty the subjective experience of a rodent, rodent models hold promise in dissecting wellconserved limbic circuits. The application of modern approaches in neuroscience has already begun to unmask the neural circuit intricacies underlying anxiety by allowing direct examination of hypotheses drawn from existing psychological concepts. This information points toward an updated conceptual model for what neural circuit perturbations could give rise to pathological anxiety, and thereby provides a roadmap for future therapeutic development.3

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The ventral hippocampus and the lateral septum work in tandem to regulate rats' open-arm exploration in the elevated plus-maze

Cited by 63 publications

References 65 publications

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

Pattern of forebrain activation in high novelty-seeking rats following aggressive encounter

Resolving the neural circuits of anxiety

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