Deep brain stimulation for enhancement of learning and memory

doi:10.1016/j.neuroimage.2013.07.066

NeuroImage

Volume 85, Part 3, 15 January 2014, Pages 996-1002

https://doi.org/10.1016/j.neuroimage.2013.07.066 Get rights and content

Highlights

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We review recent studies suggesting that DBS may be used to enhance memory.
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We discuss possible neuronal mechanisms underlying DBS related memory enhancement.
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We discuss potential of DBS treatment for memory disorders.
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We propose future directions related to DBS-enhancement of memory.

Abstract

Deep brain stimulation (DBS) has emerged as a powerful technique to treat a host of neurological and neuropsychiatric disorders from Parkinson's disease and dystonia, to depression, and obsessive compulsive disorder (Benabid et al., 1987, Lang and Lozano, 1998, Davis et al., 1997; Vidailhet et al., 2005; Mayberg et al., 2005, Nuttin et al., 1999). More recently, results suggest that DBS can enhance memory for facts and events that are dependent on the medial temporal lobe (MTL), thus raising the possibility for DBS to be used as a treatment for MTL‐ related neurological disorders (e.g. Alzheimer's disease, temporal lobe epilepsy, and MTL injuries). In the following review, we summarize key results that show the ability of DBS or cortical surface stimulation to enhance memory. We also discuss current knowledge regarding the temporal specificity, underlying neurophysiological mechanisms of action, and generalization of stimulation's effects on memory. Throughout our discussion, we also propose several future directions that will provide the necessary insight into if and how DBS could be used as a therapeutic treatment for memory disorders.

Introduction

Episodic memory, or the ability to remember personal experienced events, is severely compromised in various neurological disorders affecting the medial temporal lobe (MTL) including Alzheimer's disease, temporal lobe epilepsy, traumatic brain injury and other MTL injuries such as those occurring during stroke, cardiac arrest, or encephalitis. While deep brain stimulation (DBS) has been used to successfully treat movement disorders such as Parkinson's disease and dystonia, an exciting new frontier of DBS is the enhancement of cognitive function, and memory in particular. The implications of such enhancement to patients affected with disorders of memory may be of great significance. In the current review, we summarize several studies illustrating the potential for DBS or cortical surface stimulation to enhance episodic learning and memory. We also discuss and propose several future directions that would provide necessary insight as to whether DBS could be useful for treating memory disorders.

Section snippets

DBS of the MTL circuit enhances memory

In achieving potential enhancement of memory function by stimulation, understanding MTL circuitry is of critical importance since the ability to form episodic memories critically depends on this structure (Eichenbaum, 2000; for review see Squire et al., 2004). The human MTL consists of several functionally and structurally distinct areas including the hippocampus, amygdala, and adjacent parahippocampal, entorhinal, and perirhinal cortices. The hippocampus is comprised of even smaller

Temporal specificity of effects

Overall, an important aspect of memory enhancing DBS would be its application at a specific phase of information processing, namely during the learning, recall, or consolidation phase. Evidence from neurorehabilitation studies (Murphy and Corbett, 2009) suggests that therapeutic intervention would be ideal if used in an as-needed basis such as during learning or recall. Perhaps similarly, DBS may have larger effects depending on whether it is applied during learning (encoding), recall

Underlying neurophysiological mechanism of action

How does memory enhancing DBS affect neuronal activity at the site of delivery? Most clinical DBS studies, such as those for Parkinson's disease, stimulate nuclei or areas of gray matter. While some studies suggest that DBS of gray matter suppresses the activity of nearby neurons, others suggest that it excites afferent and/or efferent axonal projections (for review see McIntyre et al., 2004). Studies using simultaneous electrical stimulation, electrophysiology and fMRI have shown that

Generalization of effects

Thus far, studies showing DBS-related enhancement of human memory have mostly been carried out in epilepsy patients who need implantation of intracranial depth electrodes for clinical reasons. Therefore, the question remains as to whether DBS effects on memory can in fact be generalizable and extend to other patient populations (e.g. traumatic brain injury and Alzheimer's disease). Theta-frequency DBS administered to the medial septal nucleus increased hippocampal theta and improved spatial

Future directions in neuroenhancement of memory

DBS technology has the potential for significant improvement in the future. For example, a DBS system that incorporates feedback from simultaneous recording electrodes such as those recording oscillatory patterns or single neuron activity will provide more sophisticated stimulation protocols (e.g. Berger et al., 2011). Controllable DBS systems that do not utilize continuous stimulation but instead provide on-demand stimulation during periods of critical information processing may also be of

Summary and conclusions

Overall, it is necessary that future studies build upon and elucidate the mechanism of action used in DBS enhancement of memory. Clearly, the location, parameters, and phase of delivery of DBS are quite variable across studies. Thus, systematic comparisons and consistent methodologies across future studies will contribute to the understanding of DBS and its effects on learning and memory and whether it will be a useful therapeutic treatment for patients with memory disorders.

Acknowledgments

This work was supported by the National Institute of Neurological Disorders and Stroke (NS033221) and the Dana Foundation.

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Secondly, the decreased inflammatory response with VNS appears to result from NTS mediated activation of the dorsal motor nucleus and subsequent efferent pathway activation to the celiac ganglion, inhibiting cytokine production from the spleen [31]. In addition, VNS appears to improve memory when applied during learning [32–34], potentially through increased sensory gating or effects on neuroplasticity [35]. New non-invasive transcutaneous VNS (nVNS) devices have been developed that are safe, cost-effective, and portable, potentially facilitating broader adoption (e.g., at-home) and thus eliminates some of the previous limitations of implantable VNS such as high cost, surgery, and introduction of a foreign object into the patient [36,37].
Traumatic stress can have lasting effects on neurobiology and result in psychiatric conditions such as posttraumatic stress disorder (PTSD). We hypothesize that non-invasive cervical vagal nerve stimulation (nVNS) may alleviate trauma symptoms by reducing stress sympathetic reactivity. This study examined how nVNS alters neural responses to personalized traumatic scripts.
Nineteen participants who had experienced trauma but did not have the diagnosis of PTSD completed this double-blind sham-controlled study. In three sequential time blocks, personalized traumatic scripts were presented to participants immediately followed by either sham stimulation (n = 8; 0–14 V, 0.2 Hz, pulse width = 5s) or active nVNS (n = 11; 0–30 V, 25 Hz, pulse width = 40 ms). Brain activity during traumatic scripts was assessed using High Resolution Positron Emission Tomography (HR-PET) with radiolabeled water to measure brain blood flow.
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View full text

ReviewDeep brain stimulation for enhancement of learning and memory

Highlights

Abstract

Introduction

Section snippets

DBS of the MTL circuit enhances memory

Temporal specificity of effects

Underlying neurophysiological mechanism of action

Generalization of effects

Future directions in neuroenhancement of memory

Summary and conclusions

Acknowledgments

Neurosci. Biobehav. Rev.

Brain Stimul.

Neuron

Magn. Reson. Imaging

Trends Cogn. Sci.

Brain Res.

Neuron

Trends Cogn. Sci.

Electroencephalogr. Clin. Neurophysiol.

Brain Cogn.

Exp. Neurol.

Curr. Opin. Neurobiol.

Neuroscience

Brain Stimul.

Neuron

Clin. Neurophysiol.

Brain Stimul.

Lancet

Seizure

Neuroscience

Behav. Brain Res.

J. Neurosci. Methods

The Hippocampal Formation

Hippocampal Formation

Changes in apraxia after deep brain stimulation of the nucleus basalis Meynert in a patient with Parkinson dementia syndrome

Mov. Disord.

Combined (thalamotomy and stimulation) stereotactic surgery of the VIM thalamic nucleus for bilateral Parkinson's disease

Appl. Neurophysiol.

A cortical neural prosthesis for restoring and enhancing memory

J. Neural. Eng.

Stimulation of perforant path fibers induces LTP concurrently in amygdala and hippocampus in awake freely behaving rats

Neural. Plast.

Temporal lobe cortical electrical stimulation during the encoding and retrieval phase reduces false memories

PLoS One

Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory

Hippocampus

Enhanced recognition memory following vagus nerve stimulation in human subjects

Nat. Neurosci.

Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys

J. Neurophysiol.

Globus pallidus stimulation activates the cortical motor system during alleviation of Parkinsonian symptoms

Nat. Med.

The Human Hippocampus. Fuctional Anatomy, Vascularization, and Serial Sections with MRI

A cortical-hippocampal system for declarative memory

Nat. Rev. Neurosci.

Memory modulation by weak synchronous deep brain stimulation: a pilot study

Brain Stimul.

Medial temporal theta state before an event predicts episodic encoding success in humans

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

Memory enhancement induced by hypothalamic/fornix deep brain stimulation

Ann. Neurol.

A nonlinear model for hippocampal cognitive prosthesis: memory facilitation by hippocampal ensemble stimulation

IEEE Trans. Neural. Syst. Rehabil. Eng.

Stimulate or degenerate: deep brain stimulation of the nucleus basalis Meynert in Alzheimer dementia

World Neurosurg.

Review
Deep brain stimulation for enhancement of learning and memory