Nucleus basalis stimulation enhances working memory by stabilizing stimulus representations in primate prefrontal cortical activity

Qi, Xue-Lian; Liu, Ruifeng; Singh, Balbir Singh Mahinder; Bestue, David; Compte, Albert; Vazdarjanova, Almira; Blake, David T.; Constantinidis, Christos

doi:10.1016/j.celrep.2021.109469

Cited by 18 publications

(41 citation statements)

References 56 publications

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“…During the 15 s pauses, biphasic stimulation can be delivered to one or both hemispheres at intensities up to 0.5 mA, with 100 microsecond phase length, biphasic charge balanced pulses. Good effects of stimulation have been documented at 80 pulses per second during that 15 s period ( Liu et al., 2017 ; Qi et al., 2021 ). Retract the recording electrodes first from the recording chamber; when task is done then power off and disconnect the stimulator.…”

Section: Step-by-step Methods Detailsmentioning

confidence: 99%

“…Electrodes may be imaged using CT postoperatively to validate placement, but final placement should be verified histologically. We have demonstrated that these stimulation protocols improve working memory performance ( Liu et al., 2017 ; Qi et al., 2021 ), and sustained attention performance ( Liu et al., 2018 ), generate long-term neuroplasticity based effects ( Liu et al., 2017 ), and desynchronize the EEG ( Qi et al., 2021 ). During recording, for a successful stimulation we will expect to see artifacts from recording electrodes during each stimulation pulse.…”

Section: Expected Outcomesmentioning

confidence: 99%

“…We describe electrode preparation, surgery, and implantation for direct evaluation of how stimulation affects monkeys’ behavior and neuronal activity. For complete details on the use and execution of this profile, please refer to Qi et al. (2021) .…”

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confidence: 99%

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Protocol for behavioral and neural recording during stimulation of the macaque monkey nucleus basalis

Pennington

Banerjee

et al. 2022

STAR Protocols

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Summary We present an experimental protocol to record neuronal activity during intermittent stimulation of nucleus basalis (NB), as macaque monkeys perform cognitive tasks. This protocol includes implantation of electrodes and generator devices to deliver electrical stimulation to NB using multiple approaches in monkeys. Direct stimulation of NB avoids peripheral cholinergic side effects, optimizes timing, and activates non-cholinergic projection neurons. We describe electrode preparation, surgery, and implantation for direct evaluation of how stimulation affects monkeys’ behavior and neuronal activity. For complete details on the use and execution of this profile, please refer to Qi et al. (2021) .

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Section: Step-by-step Methods Detailsmentioning

confidence: 99%

Section: Expected Outcomesmentioning

confidence: 99%

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Protocol for behavioral and neural recording during stimulation of the macaque monkey nucleus basalis

Pennington

Banerjee

et al. 2022

STAR Protocols

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“…Simultaneous stimulation of the nucleus basalis and recording in downstream target areas such as the prefrontal cortex during execution of cognitive tasks ( Fig. 3 ) have also began to reveal distinct changes in neural activity that improve working memory stability [ 147 ].…”

Section: Cholinergic Dbs Stimulationmentioning

confidence: 99%

Cholinergic Deep Brain Stimulation for Memory and Cognitive Disorders

Subramaniam

Blake

Constantinidis

2021

JAD

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Memory and cognitive impairment as sequelae of neurodegeneration in Alzheimer’s disease and age-related dementia are major health issues with increasing social and economic burden. Deep brain stimulation (DBS) has emerged as a potential treatment to slow or halt progression of the disease state. The selection of stimulation target is critical, and structures that have been targeted for memory and cognitive enhancement include the Papez circuit, structures projecting to the frontal lobe such as the ventral internal capsule, and the cholinergic forebrain. Recent human clinical and animal model results imply that DBS of the nucleus basalis of Meynert can induce a therapeutic modulation of neuronal activity. Benefits include enhanced activity across the cortical mantle, and potential for amelioration of neuropathological mechanisms associated with Alzheimer’s disease. The choice of stimulation parameters is also critical. High-frequency, continuous stimulation is used for movement disorders as a way of inhibiting their output; however, no overexcitation has been hypothesized in Alzheimer’s disease and lower stimulation frequency or intermittent patterns of stimulation (periods of stimulation interleaved with periods of no stimulation) are likely to be more effective for stimulation of the cholinergic forebrain. Efficacy and long-term tolerance in human patients remain open questions, though the cumulative experience gained by DBS for movement disorders provides assurance for the safety of the procedure.

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“…Investigating the effects of NB stimulation on neuronal activity is essential for understanding its mechanism of action and optimizing its effectiveness ( Subramaniam et al, 2021 ). NB stimulation affects neuronal activity in the prefrontal cortex during performance of working memory tasks ( Qi et al, 2021 ). Reported results generally indicated an increase in mean firing rate of prefrontal neurons; however, the effects were considerably diverse, including a substantial minority of neurons being suppressed by stimulation.…”

Section: Introductionmentioning

confidence: 99%

Rhythmicity of Prefrontal Local Field Potentials after Nucleus Basalis Stimulation

Singh

Blake

et al. 2022

eNeuro

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The action of acetylcholine in the cortex is critical for cognitive functions and cholinergic drugs can improve functions such as attention and working memory. An alternative means of enhancing cholinergic neuromodulation in primates is the intermittent electrical stimulation of the cortical source of acetylcholine, the Nucleus Basalis (NB) of Meynert. NB stimulation generally increases firing rate of neurons in the prefrontal cortex, however its effects on single neurons are diverse and complex. We sought to understand how NB stimulation affects global measures of neural activity by recording and analyzing local field potentials (LFPs) in monkeys as they performed working memory tasks. NB stimulation primarily decreased power in the alpha frequency range during the delay interval of working memory tasks. The effect was consistent across variants of the task. No consistent modulation in the delay interval of the task was observed in the gamma frequency range, which has previously been implicated in the maintenance of working memory. Our results reveal global effects of cholinergic neuromodulation via deep brain stimulation, an emerging intervention for the improvement of cognitive function. Significance StatementStimulation of the endogenous source of acetylcholine in the cerebral cortex, the Nucleus Basalis (NB) of Meynert has shown promise as an alternative to cholinergic drugs, which are frontline medications for the treatment of Alzheimer's disease and age-related dementia. The neural mechanisms through which stimulation may improve cognitive function are incompletely understood. Here we investigate the effects of NB stimulation in the prefrontal cortex by examining the power of the Local Field Potentials during execution of working memory tasks.

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Nucleus basalis stimulation enhances working memory by stabilizing stimulus representations in primate prefrontal cortical activity

Cited by 18 publications

References 56 publications

Protocol for behavioral and neural recording during stimulation of the macaque monkey nucleus basalis

Protocol for behavioral and neural recording during stimulation of the macaque monkey nucleus basalis

Cholinergic Deep Brain Stimulation for Memory and Cognitive Disorders

Rhythmicity of Prefrontal Local Field Potentials after Nucleus Basalis Stimulation

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