Dentate gyrus field potentials evoked by stimulation of the basolateral amygdaloid nucleus in anesthetized rats

doi:10.1016/0006-8993(95)01465-9

Brain Research

Volume 718, Issues 1–2, 29 April 1996, Pages 53-60

https://doi.org/10.1016/0006-8993(95)01465-9 Get rights and content

Abstract

We previously found that long-term potentiation (LTP) in the dentate gyrus (DG) is attenuated by lesion of the basolateral amygdala (BLA), but it remained unclear whether or not there is neural connection between the BLA and the DG. In the present study, we tried to provide physiological evidence that the DG receives neural inputs from the BLA. Single-pulse electrical stimulation of the BLA evoked two distinct components of field potentials in the ipsilateral DG: the P1 component with 26-ms peak latency was elicited by lower intensity of BLA stimulation, whereas the P2 component with 14-ms peak latency was elicited at higher stimulus intensity. The P1 response (1) was evoked when the stimulating electrode was positioned within the BLA, (2) showed the laminar profile similar to the perforant path (PP)-evoked response and (3) exhibited strong paired-pulse facilitation. On the other hand, the P2 wave (1) was evoked even with the stimulating electrode outside the BLA, (2) did not reverse its polarity at any location in the DG and (3) showed only slight facilitation by paired-pulse stimulation. These data indicate that the P1 component represents synaptic responses of DG granule cells to neural inputs from the BLA. Furthermore, the BLA-evoked DG field potentials were not affected by local injection of tetracaine into the PP and displayed LTP independently of the PP-evoked response, suggesting that neural inputs from the BLA are not mediated by the PP.

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Adrenergic β receptor activation in the basolateral amygdala, which is intracellular Zn<sup>2+</sup>-dependent, rescues amyloid β<inf>1-42</inf>-induced attenuation of dentate gyrus LTP
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Citation Excerpt :
This modulation is linked with response of the stress hormones, i.e., noradrenaline and corticosterone, in many cases, resulting in establishing memory of diverse experience (Akirav and Richter-Levin, 2002). Reinforcement of dentate gyrus LTP has been shown to depend on noradrenergic and cholinergic activation under low or moderate stress conditions (Ikegaya et al., 1997; Frey et al., 2001; Straube et al., 2003) and can be modulated by the BLA (Ikegaya et al., 1996, 1997; Almaguer-Melian et al., 2003; Nakao et al., 2004). Dentate gyrus LTP maintenance can be influenced by the BLA through different mechanisms: a short-lasting corticosterone-dependent and β-adrenergic-independent mechanism and a long-lasting mechanism facilitated by hippocampal β-adrenergic mechanisms (Korz and Frey, 2005).
On the basis of the evidence that the basolateral amygdala (BLA) modulates hippocampal memory processes via synaptic plasticity, here we report that adrenergic β receptor activation in the BLA rescues amyloid β_1-42 (Aβ_1-42)-induced attenuation of long-term potentiation (LTP) at perforant pathway-dentate granule cell (DGC) synapses. When 500 μM isoproterenol (2 μl), an adrenergic β receptor agonist, was injected into the BLA 20 min before LTP induction, LTP was enhanced. Isoproterenol-mediated enhancement of LTP was blocked by co-injection with 100 μM ZnAF-2DA, an intracellular Zn²⁺ chelator, suggesting that intracellular Zn²⁺ is required for the intracellular signaling cascade after adrenergic β receptor activation in the BLA. Aβ_1-42-induced attenuation of LTP, which was induced by Aβ_1-42 injection into the dentate gyrus 60 min before LTP induction, was rescued by isoproterenol injection into the BLA 20 min before LTP induction, but not by 500 μM phenylephrine (2 μl), an adrenergic α₁ receptor agonist, injection into the BLA, which did not enhance LTP unlike the case of isoproterenol injection. Interestingly, Aβ_1-42-induced attenuation of LTP was also rescued by 100 μM isoproterenol injection into the BLA 20 min before LTP induction, which did not enhance LTP. The present study demonstrates that adrenergic β receptor activation in the BLA, which is linked with intracellular Zn²⁺ signaling, rescues Aβ_1-42-induced attenuation of dentate gyrus LTP. It is likely that adrenergic β receptor activation in the BLA is a strategy for rescuing Aβ_1-42-induced cognitive decline that is associated with hippocampal synaptic plasticity.
Orexin 1 and orexin 2 receptor antagonism in the basolateral amygdala modulate long-term potentiation of the population spike in the perforant path-dentate gyrus-evoked field potential in rats
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Involvement of amygdalo-hippocampal substructures in patients with narcolepsy due to deficiencies in the orexinergic system, and the presence of hippocampus-dependent memory impairments in this disorder, have led us to investigate the effects of orexin 1 and 2 receptor antagonism in the basolateral amygdala (BLA) on long-term potentiation (LTP) of dentate gyrus (DG) granular cells. We used a 200-Hz high-frequency stimulation protocol in anesthetized rats. We studied the long-term synaptic plasticity of perforant path-dentate gyrus granule cells following the inactivation of orexin receptors before and after tetanic stimulation. LTP of the DG population spike was attenuated in the presence of orexin 1 and 2 receptor antagonism (treatment with SB-334867-A and TCS-OX2–29, respectively) in the BLA when compared to that observed following treatment with dimethyl sulfoxide (DMSO). However, the population excitatory post-synaptic potentials were not affected. Moreover, when orexin 1 and 2 receptors in the BLA were blocked after LTP induction, there were no differences between the DMSO and treatment groups. Our findings suggest that the orexinergic system of the BLA plays a modulatory role in the regulation of hippocampal plasticity in rats.
Blockade of intracellular Zn<sup>2+</sup> signaling in the basolateral amygdala affects object recognition memory via attenuation of dentate gyrus LTP
2017, Neurochemistry International
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Twenty minutes later, LTP was induced by delivery of high-frequency stimulation (HFS; 5 trains of 400 pulses at 400 Hz separated by 2 min) and PS amplitudes were recorded for 60 min. In vivo LTP at BLA-DGC synapses was recorded according to the method reported previously (Ikegaya et al., 1996; Abe et al., 2008). Male rats were anesthetized with chloral hydrate (400 mg/kg) and placed in a stereotaxic apparatus.
Hippocampus-dependent memory is modulated by the amygdala. However, it is unknown whether intracellular Zn²⁺ signaling in the amygdala is involved in hippocampus-dependent memory. On the basis of the evidence that intracellular Zn²⁺ signaling in dentate granule cells (DGC) is necessary for object recognition memory via LTP at medial perforant pathway (PP)-DGC synapses, the present study examined whether intracellular Zn²⁺ signaling in the amygdala influences object recognition memory via modulation of LTP at medial PP-DGC synapses. When ZnAF-2DA (100 μM, 2 μl) was injected into the basolateral amygdala (BLA), intracellular ZnAF-2 locally chelated intracellular Zn²⁺ in the amygdala. Recognition memory was affected when training of object recognition test was performed 20 min after ZnAF-2DA injection into the BLA. Twenty minutes after injection of ZnAF-2DA into the BLA, LTP induction at medial PP-DGC synapses was attenuated, while LTP induction at PP-BLA synapses was potentiated and LTP induction at BLA-DGC synapses was attenuated. These results suggest that intracellular Zn²⁺ signaling in the BLA is involved in BLA-associated LTP and modulates LTP at medial PP-DGC synapses, followed by modulation of object recognition memory.
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In recent years, both major depression and antidepressant therapy have been linked to adult hippocampal neurogenesis. The hippocampus is not a homogeneous brain area, and a converging body of evidence indicates a functional dissociation along its septo-temporal axis, the dorsal part being involved more in learning/memory and spatial navigation, while the ventral sub-region is linked more to emotional behavior and regulation of the neuroendocrine stress axis. Research has therefore been conducted in an attempt to relate effects of models of depression and of antidepressant therapies to adult neurogenesis along the septo-temporal axis of the hippocampus. The present paper reviews the current literature addressing this question and discusses the possible mechanisms involved and the functional significance of such regional effects. This review shows that animal models of depression elicit an effect restricted to the ventral hippocampus more frequently than a dorsal-specific effect. However, this is also stage specific, and concerns neurogenesis, rather than cell proliferation or survival. Surprisingly, the same does not apply regarding the effects of selective serotonin re-uptake inhibitors that act in a more uniform way on dorsal and ventral adult neurogenesis in most studies. Some recently introduced clinical compounds (e.g., agomelatine) or putative antidepressants have a specific action on the ventral sub-region, indicating that an action restricted to this part of the brain may be sufficient to achieve remission. Finally, non-pharmacological manipulations that are also endowed with antidepressant effects, such as environmental enrichment or physical exercise, also act on both subdivisions, although some studies pointed to specificity of dorsal neurogenesis. The different treatments, acting either on the dorsal or on the ventral sub-regions, could promote recovery by improving either ventral- or dorsal-related functions, both contributing in a different way to treatment efficacy.
The Brain on Stress: Vulnerability and Plasticity of the Prefrontal Cortex over the Life Course
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Citation Excerpt :
The prefrontal cortex, amygdala, and hippocampus are interconnected and influence each other via direct and indirect neural activity (Akirav and Richter-Levin, 1999; Ghashghaei and Barbas, 2002; McDonald, 1987; Mcdonald et al., 1996; Petrovich et al., 2001). For example, inactivation of the amygdala blocks stress-induced impairment of hippocampal LTP and spatial memory (Kim et al., 2005) and stimulation of basolateral amygdala enhances dentate gyrus field potentials (Ikegaya et al., 1996), while stimulation of medial prefrontal cortex decreases responsiveness of central amygdala output neurons (Quirk et al., 2003). The processing of emotional memories with contextual information requires amygdala-hippocampal interactions (Phillips and LeDoux, 1992; Richardson et al., 2004), whereas the prefrontal cortex, with its powerful influence on amygdala activity (Quirk et al., 2003), plays an important role in fear extinction (Milad and Quirk, 2002; Morgan and LeDoux, 1995).
The prefrontal cortex (PFC) is involved in working memory and self-regulatory and goal-directed behaviors and displays remarkable structural and functional plasticity over the life course. Neural circuitry, molecular profiles, and neurochemistry can be changed by experiences, which influence behavior as well as neuroendocrine and autonomic function. Such effects have a particular impact during infancy and in adolescence. Behavioral stress affects both the structure and function of PFC, though such effects are not necessarily permanent, as young animals show remarkable neuronal resilience if the stress is discontinued. During aging, neurons within the PFC become less resilient to stress. There are also sex differences in the PFC response to stressors. While such stress and sex hormone-related alterations occur in regions mediating the highest levels of cognitive function and self-regulatory control, the fact that they are not necessarily permanent has implications for future behavior-based therapies that harness neural plasticity for recovery.
The expression of non-clustered protocadherins in adult rat hippocampal formation and the connecting brain regions
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Non-clustered protocadherins (PCDHs) are calcium-dependent adhesion molecules which have attracted attention for their possible roles in the neuronal circuit formation during development and their implications in the neurological disorders such as autism and mental retardation. Previously, we found that a subset of the non-clustered PCDHs exhibited circuit-dependent expression patterns in thalamo-cortical connections in early postnatal rat brain, but such patterns disappeared in adulthood. In this study, we identified that the non-clustered PCDHs showed differential expression patterns along the septotemporal axis in the subregions of adult hippocampus and dentate gyrus with topographical preferences. The expressions of PCDH1, PCDH9, PCDH10 and PCDH20 showed septal preferences, whereas the expressions of PCDH8, PCDH11, PCDH17 and PCDH19 showed temporal preferences, suggesting that they play roles in the formation/maintenance of intrahippocampal circuits. PCDHs also exhibited the region-specific expression patterns in the areas connected to hippocampal formation such as entorhinal cortex, lateral septum, and basolateral amygdaloid complex. Furthermore, the expression levels of three PCDHs (PCDH8, PCDH19 and PCDH20) were regulated by the electroconvulsive shock stimulation of the brain in the adult hippocampus and dentate gyrus. These results suggest that non-clustered PCDHs are involved in the maintenance and plasticity of adult hippocampal circuitry.

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Dentate gyrus field potentials evoked by stimulation of the basolateral amygdaloid nucleus in anesthetized rats

Abstract

Trends Neurosci.

Brain Res.

Brain Res.

Neurosci. Res.

Neurosci. Res.

Behav. Brain Res.

Brain Res.

Brain Res.

Interhippocampal impulses II. Apical dendritic activation of CAI neurons

Acta Physiol. Scand.

A synaptic model of memory: long-term potentiation in the hippocampus

Nature

The functional anatomy of amygdala efferent pathways

Soc. Neurosci. Abstr.