Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Seager, Matthew A.; Johnson, Lynn D.; Chabot, Elizabeth S.; Asaka, Yukiko; Berry, Stephen D.

doi:10.1073/pnas.032662099

Cited by 185 publications

(203 citation statements)

References 69 publications

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“…Based on experimental observations in rats, theta oscillation of the hippocampal formation is commonly regarded as a physiological encoding frequency in memory formation (Buzsaki, 2002;Jensen and Tesche, 2002;Seager et al, 2002). In addition, recent observation of human theta has strengthened the connection between theta oscillation and cognitive processes.…”

Section: Introductionmentioning

confidence: 99%

Norepinephrine but not Serotonin Reuptake Inhibitors Enhance Theta and Gamma Activity of the Septo-Hippocampal System

Hajós¹,

Hoffmann²,

Robinson³

et al. 2002

Neuropsychopharmacol

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Current neurobiological concepts attribute a central role of the hippocampal formation in cognitive and affective processes. Recent studies indicate that the hippocampus is affected in human depression, and antidepressant drugs induce hippocampal adaptive changes that are thought to be associated with their therapeutic action. In the present study, we investigated the action of various antidepressant drugs on the activity of the septo-hippocampal system, its oscillatory activity in particular. The acute effects of the norepinephrine (NE) reuptake inhibitors reboxetine and desipramine, and the selective serotonin reuptake inhibitor fluvoxamine were evaluated. Extracellular single-unit recordings were performed from the medial septum/diagonal band of Broca (MS/DBv), with simultaneous hippocampal EEG recordings of anesthetized rats. Systemic administration of reboxetine synchronized hippocampal EEG, resulting in a significant increase in power at theta frequency, and an increase in frequency and power of gamma-wave activity. Parallel to EEG synchrony, reboxetine induced or enhanced theta oscillation of MS/DBv neurons. Oscillatory frequencies of MS/DBv neurons were identical, and phase locked to the corresponding hippocamapal theta frequencies. Under the same experimental conditions, reboxetine induced a two-fold increase in extracellular NE (but not serotonin) levels in the hippocampus as revealed by microdialysis. Desipramine, but not the serotonin reuptake inhibitor fluvoxamine, evoked responses similar to those of reboxetine regarding septo-hippocampal theta activity. The present findings indicate that even though both NE and serotonin reuptake inhibitors are clinically effective antidepressant drugs, their action on the septo-hippocampal oscillatory behavior is different. It is presumed that selective NE reuptake inhibitors could modulate various cognitive processes associated with hippocampal oscillatory activity.

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Section: Introductionmentioning

confidence: 99%

Norepinephrine but not Serotonin Reuptake Inhibitors Enhance Theta and Gamma Activity of the Septo-Hippocampal System

Hajós¹,

Hoffmann²,

Robinson³

et al. 2002

Neuropsychopharmacol

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“…Previous work has shown that reducing Theta amplitude by pharmacological means impairs performance in WM tasks, thereby demonstrating that Theta most likely plays a functional role in the WM storage system (Givens andOlton 1990, 1995). Other studies have shown that the learning of an eye blink classical conditioning task is much reduced when stimulation occurs in the absence of Theta, while stimulation only in the presence of Theta produced good learning results (Seager et al 2002;Griffin et al 2004).…”

mentioning

confidence: 98%

“…The reduction or block of Theta rhythm interferes with the performance in various WM tasks (Winson 1978;Givens andOlton 1990, 1995), and the amplitude of Theta correlated with the ability to perform well in WM tasks (Klimesch et al 2001;Seager et al 2002;Griffin et al 2004). It appears counter-intuitive that higher amplitudes of Theta would reduce performance in WM tasks.…”

Section: How Can Increased Theta Affect Wm?mentioning

confidence: 99%

Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory

Hölscher

Schmid²,

Pilz³

et al. 2005

Learn. Mem.

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Metabotropic glutamate receptors (mGluRs) are known to play a role in synaptic plasticity and learning. We have previously shown that mGluR7 deletion in mice produces a selective working memory (WM) impairment, while other types of memory such as reference memory remain unaffected. Since WM has been associated with Theta activity (6-12 Hz) in EEGs, and since EEG abnormalities have been observed in these mice before, we studied the effect of mGluR7 gene ablation on EEG activity in the hippocampus, in particular in the Theta range, during performance of a WM task. In an eight-arm maze with four arms baited, mGluR7 knock-out (KO) and wild-type mice committed the same number of reference memory errors, whereas KOs committed more WM errors. While performing the task, KO mice showed substantially higher Theta amplitudes, and the ratio of Theta to overall EEG power was much increased. No change was seen in the Delta (0-5 Hz), or Gamma (30-40 Hz) EEG bands compared with controls. When recording EEGs during periods of rest in the home cages, no difference was seen between groups. These findings suggest that mGluR7 is important for modulation and control of Theta activity. Since only WM was affected, and only the Theta range of EEG activity was altered, these results show a correlation between Theta rhythm and WM performance, and therefore support the concept that Theta activity in the hippocampus is involved in WM storage.Metabotropic glutamate receptors (mGluRs) are a family of glutamate-sensitive receptors that are coupled to intracellular signal transduction via G-proteins (Pin and Duvoisin 1995). It is known that mGluRs play an important role in the regulation of CNS synaptic plasticity, and also in some processes of memory formation. Pharmacological blockade of mGluR group III receptors (subtypes 4, 6, 7, and 8) has profound effects on the induction of synaptic plasticity (Bashir et al. 1993;Richter-Levin et al. 1994;Hölscher et al. 1997a), synaptic depression (Manahan-Vaughan 2000;Weber et al. 2002), and spatial learning (Hölscher et al. 1996(Hölscher et al. , 1999.In a previous study, we tested the effect of mGluR7 deletion on different forms of learning and memory formation (Hölscher 2003). We showed that mGluR7-deficient (knock-out; KO) mice were not impaired in a non-associative habituation task or in performing reference memory tasks of different complexities (open field, T-maze, four-and eight-arm mazes). However, in tasks that require increased capacity of working memory (WM) performance, mGluR7 KO mice showed clear deficits.WM contains task-related information required to develop plans of action and to guide behavior (Baddeley and Hitch 1974;Olton et al. 1979). In the present paper, we adhere to the definition of WM by Olton et al. (1979), who emphasized the importance of hippocampal activity for supporting WM. How WM is actually encoded and stored in the brain has been under investigation for a long time. The occurrence of oscillations in the EEG of subjects that performed WM tasks had been observed. In pa...

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“…By comparing the performance of two groups of animals to yoked controls trained with matched intertrial intervals, it was found that instead of theta benefiting learning, rather nontheta was especially detrimental in tasks that do not require the hippocampus such as delay conditioning. Pre-task theta activity was strongly associated with the subsequent learning rate in operant conditioning [130]. Whereas cerebellar and oculomotor pathways are clearly essential substrates of eyeblink conditioning, hippocampal influences appear to be parallel and modulatory in nature.…”

Section: Frequency-contingent Learningmentioning

confidence: 95%

“…The theta rhythm (usually defined as 4-8 Hz in humans, and as 3-10 Hz in animals) is known to enhance hippocampal plasticity and accelerate learning in rats, cats, rabbits, and other animal species [67], and thus manipulations based on theta activity could be used to counteract impairments in learning due to abnormal development, aging or pathology of the hippocampus and other memory structures. Rabbits that receive training trials in the presence of theta were found to learn twice as fast as those receiving trials in the absence of theta [130]. By comparing the performance of two groups of animals to yoked controls trained with matched intertrial intervals, it was found that instead of theta benefiting learning, rather nontheta was especially detrimental in tasks that do not require the hippocampus such as delay conditioning.…”

Section: Frequency-contingent Learningmentioning

confidence: 96%

Techniques and devices to restore cognition

Serruya

Kahana

2008

Behavioural Brain Research

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Executive planning, the ability to direct and sustain attention, language and several types of memory may be compromised by conditions such as stroke, traumatic brain injury, cancer, autism, cerebral palsy and Alzheimer's disease. No medical devices are currently available to help restore these cognitive functions. Recent findings about the neurophysiology of these conditions in humans coupled with progress in engineering devices to treat refractory neurological conditions imply that the time has arrived to consider the design and evaluation of a new class of devices. Like their neuromotor counterparts, neurocognitive prostheses might sense or modulate neural function in a non-invasive manner or by means of implanted electrodes. In order to paint a vision for future device development, it is essential to first review what can be achieved using behavioral and external modulatory techniques. While non-invasive approaches might strengthen a patient's remaining intact cognitive abilities, neurocognitive prosthetics comprised of direct brain-computer interfaces could in theory physically reconstitute and augment the substrate of cognition itself.

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Oscillatory brain states and learning: Impact of hippocampal theta-contingent training

Cited by 185 publications

References 69 publications

Norepinephrine but not Serotonin Reuptake Inhibitors Enhance Theta and Gamma Activity of the Septo-Hippocampal System

Norepinephrine but not Serotonin Reuptake Inhibitors Enhance Theta and Gamma Activity of the Septo-Hippocampal System

Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory

Techniques and devices to restore cognition

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