The role of the ventral dentate gyrus in anxiety-based behaviors

Weeden, Christy S. S.; Roberts, Jared M.; Kamm, Allison M.; Kesner, Raymond P.

doi:10.1016/j.nlm.2014.12.002

Cited by 69 publications

(63 citation statements)

References 39 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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“…However, later studies using more selective, fiber-sparing lesions of the ventral hippocampus also found decreased anxiety-like behavior in unconditioned exploratory tasks; these selectively-lesioned animals spend more time exploring open arms of the elevated plus maze, more time exploring the center of an open field, and less time to begin feeding in a neophagia task (Bannerman et al 2002, 2003; Deacon et al 2002; Kjelstrup et al 2002). Similar decreases in anxiety-like behavior in the elevated plus maze and open field have been observed in mice lacking functional N -methyl-D-aspartate (NMDA) receptors in dentate gyrus granule cells (Barkus et al 2010) and in rats with ventral dentate gyrus lesions (Weeden 2012), suggesting that loss of functional granule neurons mimics loss of the entire hippocampus. In addition, ventral hippocampus-lesioned animals show decreased freezing behavior in response to an innate/unlearned stimulus (cat odor) as well as to a conditioned stimulus, either a cue or context previously associated with shock (Pentkowski et al 2006, Richmond et al 1999).…”

Section: Hippocampus-dependent Behaviors Without Clear Memory Componentsmentioning

confidence: 62%

Adult Neurogenesis: Beyond Learning and Memory

Cameron

Glover

2015

Annu. Rev. Psychol.

242

166

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New neurons continue to be generated in the dentate gyrus throughout life, providing this region of the hippocampus with exceptional structural plasticity, but the function of this ongoing neurogenesis is unknown. Inhibition of adult neurogenesis produces some behavioral impairments that suggest a role for new neurons in learning and memory, however other behavioral changes appear inconsistent with this function. A review of studies investigating the function of the hippocampus going back several decades reveals many ideas that seem to converge on a critical role for the hippocampus in stress response and emotion. These potential hippocampal functions provide new avenues for investigating the behavioral functions of adult neurogenesis. And, conversely, studies in animals lacking adult neurogenesis, which are likely to have more limited and more specific impairments than those produced by lesions, may provide valuable new insights into the function of the hippocampus. A complete understanding of the function of the hippocampus must explain its role in emotion and the relationship between its emotional and memory functions.

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“…However, use of the terms fear learning, fear conditioning, fear-motivated learning, fear memory, and fear extinction has become so widespread that many readers interested in these subjects might well skip altogether an article whose title does not contain those words. So they will be used here as they are in most other recent accounts of the subject (95,98,115,116,182,294,296,299,378,403,421,462,463,468,475,501,524,653).…”

Section: B Fear-motivated Learningmentioning

confidence: 99%

“…The LA (448) and BLA (380), microcircuits within the amygdala including the CE (153,475), the hippocampus (265,657) including the DG (524,574,653), the vmPFC which is tightly linked to the preceding structures (335,336,421), and some other areas of the neocortex [anterior (68,215,457,587) and posterior cingulate (610), posterior parietal (445) and retrosplenial (140)] are involved in fear learning and extinction as well as in the retrieval of fearmotivated behaviors (FIGURE 4). In IA, the main site of consolidation is the CA1 region of the hippocampus, and the mechanism involves LTP (657).…”

Section: Summing Upmentioning

confidence: 99%

Fear Memory

Izquierdo

Furini

Myskiw

2016

Physiological Reviews

380

259

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Fear memory is the best-studied form of memory. It was thoroughly investigated in the past 60 years mostly using two classical conditioning procedures (contextual fear conditioning and fear conditioning to a tone) and one instrumental procedure (one-trial inhibitory avoidance). Fear memory is formed in the hippocampus (contextual conditioning and inhibitory avoidance), in the basolateral amygdala (inhibitory avoidance), and in the lateral amygdala (conditioning to a tone). The circuitry involves, in addition, the pre-and infralimbic ventromedial prefrontal cortex, the central amygdala subnuclei, and the dentate gyrus. Fear learning models, notably inhibitory avoidance, have also been very useful for the analysis of the biochemical mechanisms of memory consolidation as a whole. These studies have capitalized on in vitro observations on long-term potentiation and other kinds of plasticity. The effect of a very large number of drugs on fear learning has been intensively studied, often as a prelude to the investigation of effects on anxiety. The extinction of fear learning involves to an extent a reversal of the flow of information in the mentioned structures and is used in the therapy of posttraumatic stress disorder and fear memories in general.

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The role of the ventral dentate gyrus in anxiety-based behaviors

Cited by 69 publications

References 39 publications

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

Dissecting the Function of Hippocampal Oscillations in a Human Anxiety Model

Adult Neurogenesis: Beyond Learning and Memory

Fear Memory

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