Effects of Blood Estrogen Level on Cortical Activation Patterns during Cognitive Activation as Measured by Functional MRI

Dietrich, Thomas; Krings, Timo; Neulen, J.; Hinckeldey, Klaus Willmes-von; Erberich, Stephan G.; Thron, A.; Sturm, Walter

doi:10.1006/nimg.2001.0703

Cited by 205 publications

(117 citation statements)

References 26 publications

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“…These rapid actions of estrogens appear to explain the observation that in pre-, peri-, and postmenopausal women, estrogens affect neuronal activity measured by fMRI in a variety of brain regions during the performance of cognitive (39) and sustained attentional (40) tasks. Furthermore, estrogens enhance visual and place memory (41) and working memory performances in rats (42) and facilitate cholinergic neurotransmission in the septal-hippocampal pathways (43).…”

Section: Discussionmentioning

confidence: 99%

Estrogens directly potentiate neuronal L-type Ca ²⁺ channels

Sarkar

Huang

Logan

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

100

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L-type voltage-gated Ca 2؉ channels (VGCC) play an important role in dendritic development, neuronal survival, and synaptic plasticity. Recent studies have demonstrated that the gonadal steroid estrogen rapidly induces Ca 2؉ influx in hippocampal neurons, which is required for neuroprotection and potentiation of LTP. The mechanism by which estrogen rapidly induces this Ca 2؉ influx is not clearly understood. We show by electrophysiological studies that extremely low concentrations of estrogens acutely potentiate VGCC in hippocampal neurons, hippocampal slices, and HEK-293 cells transfected with neuronal L-type VGCC, in a manner that was estrogen receptor (ER)-independent. Equilibrium, competitive, and whole-cell binding assays indicate that estrogen directly interacts with the VGCC. Furthermore, a L-type VGCC antagonist to the dihydropyridine site displaced estrogen binding to neuronal membranes, and the effects of estrogen were markedly attenuated in a mutant, dihydropyridineinsensitive L-type VGCC, demonstrating a direct interaction of estrogens with L-type VGCC. Thus, estrogen-induced potentiation of calcium influx via L-type VGCC may link electrical events with rapid intracellular signaling seen with estrogen exposure leading to modulation of synaptic plasticity, neuroprotection, and memory formation.estrogen receptors ͉ signaling ͉ estradiol ͉ memory A large body of evidence shows that estrogens exert multiple rapid effects on the structure and function of neurons in a variety of brain regions, including the hippocampus (1). For example, estrogens rapidly potentiate kainite-induced currents in hippocampal neurons from wild-type (2) as well as from estrogenreceptor (ER)-␣ knockout (3) mice and induce rapid spine synapse formation in the CA1 hippocampus of ovariectomized (OVX) rats (4). Furthermore, acute application of estrogens to hippocampal slices increases NMDA and AMPA receptor transmission (5), induces long-term potentiation (LTP) and long-term depression (LTD) (6), and rapidly modulates neuronal excitability in rat medial amygdala (7) and hippocampus(8).It is well known that estrogens interact with cell membrane components and initiate signaling events leading to a rise in intracellular Ca 2ϩ , and activation of Src kinase, G protein-coupled receptor (GPCR), MAPK, PI3K/AKT, PKA, and adenylyl cyclase (9). The mechanism(s) by which estrogens induce these rapid and diverse effects remains largely unknown. Ca 2ϩ is a second messenger that can trigger the modification of synaptic efficacy. A plasticity-induction protocol like repetitive low-frequency synaptic stimulation (10) induces the elevation of postsynaptic intracellular Ca 2ϩ . The level of intracellular Ca 2ϩ concentration can activate numerous kinases like CAMK, PKA, PKC, MAPK, PI3K, or phosphatases (11-15), which, respectively, phosphorylate or dephosphorylate ion channels, transcription factors, and other proteins that are involved in synaptic plasticity and memory formation. Because voltage-gated Ca 2ϩ channels (VGCC)-mediated extracellular Ca ...

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Section: Discussionmentioning

confidence: 99%

Estrogens directly potentiate neuronal L-type Ca ²⁺ channels

Sarkar

Huang

Logan

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

100

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“…Following the theory, estrogen may have an impact on hemispheric dominance that eventually relates to performance on a mental rotation task. However, there have been some inconsistent findings that support the theory (Dietrich et al, 2001;Halari et al, 2006). Further research should address how estrogen relates to performance on mental rotation tasks.…”

Section: Discussionmentioning

confidence: 99%

Relationships between Salivary Estradiol and Components of Mental Rotation in Young Men

Kozaki

Yasukouchi

2008

J Physiol Anthropol

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Testosterone and estradiol levels were measured by saliva assays in 15 young men, and their relationships with different processes in a mental rotation task were elucidated. The estradiol level was positively correlated with reaction time; this effect was yielded by the slope of functions relating performance to angular disparity. These findings suggest that estrogen may inhibit the performance of a mental rotation task by affecting perception of the rotation process.

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“…There have been few neuroimaging studies exploring differences across the menstrual cycle (51)(52)(53). One fMRI study of the menstrual cycle used a semantic decision language task contrasted with a letter-matching perceptual task (53).…”

Section: Discussionmentioning

confidence: 99%

“…One fMRI study of the menstrual cycle used a semantic decision language task contrasted with a letter-matching perceptual task (53). Another had all subjects perform a word-stem completion task, a mental rotation task, and a simple motor task (52). In both of these studies, menstrual cycle phase had strong effects on the size of brain activations related to the cognitive tasks but had little effect on the brain activity related to the perceptual or motor tasks.…”

Section: Discussionmentioning

confidence: 99%

Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle

Protopopescu

Pan²,

Altemus³

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

187

128

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The orbitofrontal cortex (OFC) has been implicated in the representation of emotional stimuli, assignment of emotional valence͞ salience to stimuli, stimulus-reinforcement association learning, motivation, and socio-emotional control. Using functional magnetic resonance imaging in female subjects without premenstrual mood symptoms, we found that OFC activity to emotional linguistic stimuli varies depending on the menstrual cycle phase. Specifically, anterior-medial OFC activity for negative vs. neutral stimuli was increased premenstrually and decreased postmenstrually. The inverse pattern was seen in the lateral OFC. These findings suggest that specific subregional OFC activity to emotional stimuli is modulated across the menstrual cycle. The data also demonstrate that menstrual cycle phase is an important consideration in further studies attempting to elucidate the neural substrates of affective representation.functional MRI ͉ brain ͉ mood ͉ emotion ͉ women D espite a vast literature describing sex hormone influences on the central nervous system and a growing emotional neuroscience literature, there are few data concerning the effects of menstrual cycle phase on the neurobiology of emotional processing in humans. This neuroimaging study specifically probes emotion and limbic activity across the menstrual cycle in women carefully characterized as having no premenstrual mood symptoms. Our results implicate the orbitofrontal cortex (OFC) as a key limbic region in which activity in response to emotional stimuli and behavioral demands is influenced by menstrual cycle phase.Damage to the OFC has long been associated with socioemotional dyscontrol (1-4). Patients with OFC lesions are prone to disadvantageous decision-making, perhaps because of an inability to evoke appropriate somatic-feeling states that would inform advantageous response selection. The OFC has been implicated in inhibitory control and emotional regulation, and has been hypothesized to have a specific role in emotion-influenced decision making (5-7).There is abundant evidence for OFC involvement in motivational operations (8). Rapid stimulus-reinforcement association learning is implemented in the OFC (8), and the OFC is important for the alteration of stimulus-reward associations (9). The OFC appears to respond to the pleasantness of some stimuli (10, 11) as well as to the unpleasantness of other stimuli (8,(12)(13)(14)(15).Regarding emotional processing, a metaanalysis of functional neuroimaging studies on OFC function supports a medio-lateral gradient for representation of positive and negative stimuli, respectively, and an anterio-posterior gradient for complex (higher-order͞ polymodal) and simple (lower-order͞unimodal) stimuli, respectively (16). However, some studies have found medial OFC activity to negative stimuli or lateral OFC activity to positive stimuli (17)(18)(19). Key issues in understanding these discrepancies include sensory modalities of presented stimuli, stimulus characteristics that may confound valence differences, and individu...

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Effects of Blood Estrogen Level on Cortical Activation Patterns during Cognitive Activation as Measured by Functional MRI

Cited by 205 publications

References 26 publications

Estrogens directly potentiate neuronal L-type Ca ²⁺ channels

Estrogens directly potentiate neuronal L-type Ca ²⁺ channels

Relationships between Salivary Estradiol and Components of Mental Rotation in Young Men

Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle

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Effects of Blood Estrogen Level on Cortical Activation Patterns during Cognitive Activation as Measured by Functional MRI

Cited by 205 publications

References 26 publications

Estrogens directly potentiate neuronal L-type Ca 2+ channels

Estrogens directly potentiate neuronal L-type Ca 2+ channels

Relationships between Salivary Estradiol and Components of Mental Rotation in Young Men

Orbitofrontal cortex activity related to emotional processing changes across the menstrual cycle

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Product

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Estrogens directly potentiate neuronal L-type Ca ²⁺ channels

Estrogens directly potentiate neuronal L-type Ca ²⁺ channels