Material-Specific Recognition Memory Deficits Elicited by Unilateral Hippocampal Electrical Stimulation

Coleshill, Steven G.; Binnie, C.D.; Morris, Robin G.; Alarcón, Gonzalo; Boas, W. van Emde; Velis, Demetrios N.; Simmons, Andy; Polkey, Charles E.; Veelen, C.W.M. van; Rijen, Peter C. van

doi:10.1523/jneurosci.4352-03.2004

Cited by 120 publications

(84 citation statements)

References 49 publications

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“…Standardized neuropsychological examination in our study, however, revealed mildly or moderately impaired verbal long-term memory in patients with left HI, and nonverbal long-term memory deficits in patients with right HI. These memory deficits are in line with other temporal lobe pathologies, as described by lesional studies, 20 functional studies with transient unilateral hippocampal electric stimulation in epilepsy patients, 21 or functional MRI studies. 22 These are cognitive areas that may well escape a standard neurological examination in acute stroke patients, which focuses on the most common items defined in the NIH stroke scale.…”

Section: Discussionsupporting

confidence: 84%

Hippocampal Lesion Patterns in Acute Posterior Cerebral Artery Stroke

Szabo

Förster

Jäger

et al. 2009

Stroke

115

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Background and Purpose-Reports of ischemic stroke affecting the hippocampus are rare. In this study we used diffusion-weighted MRI (DWI) to characterize patients with posterior circulation stroke involving the hippocampus. Methods-Fifty-seven consecutive acute stroke patients with hippocampal infarct (HI) on DWI were analyzed with regard to clinical features and ischemic lesion patterns. The last 20 of these underwent additional neuropsychological testing of short-term, working, and episodic long-term memory. Results-We found unilateral HI in 54 and bilateral HI in 3 patients. Visual analysis identified 4 patterns of DWI lesion affecting (1) the complete hippocampus (15/60), (2) the lateral (19/60) or (3) dorsal (22/60) parts of the hippocampal body and tail, and (4) circumscribed lesions in the lateral hippocampus (4/60), corresponding well to hippocampal vascular anatomy. In all cases DWI showed further ischemic lesions in the posterior circulation. Symptoms from lesions outside the hippocampus were the common leading clinical signs. Whereas mnestic deficits were prominent in only 11/57 patients, neuropsychological examination in 20 patients showed deficits of verbal episodic long-term memory in left and of nonverbal episodic long-term memory in right HI. Conclusion-Several phenotypic lesion patterns can be distinguished in HI that usually occur as part of multifocal PCA ischemia. A careful neuropsychological examination is necessary to detect resulting memory deficits.

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Section: Discussionsupporting

confidence: 84%

Hippocampal Lesion Patterns in Acute Posterior Cerebral Artery Stroke

Szabo

Förster

Jäger

et al. 2009

Stroke

115

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“…Sobotka et al (2005) also showed recently that delay-interval ES directly in the monkey hippocampus, persisting for 125-250 ms but delivered 1 s after onset of the sample stimulus, disrupts recognition in a short-term delayed matching-to-sample task. Their findings, in conjunction with our own and those of Coleshill et al (2004), suggest that the hippocampus may be differentially engaged, or controlled, in long-term versus short-term (working) memory tasks.…”

Section: Discussionsupporting

confidence: 67%

“…Impairments to subsequent recognition ability attributable to disruption of hippocampal encoding activity have been reported in a recent experiment by Coleshill et al (2004) that used subepileptogenic electrical stimulation (ES) applied directly to the hippocampus in human epilepsy patients. ES was time locked to the presentation of visual stimuli during the encoding phase of a recognition memory task similar to the one we used in the present experiments, resulting in recognition impairments for such items compared with items presented for encoding without concurrent ES.…”

Section: Discussionmentioning

confidence: 99%

Retrieval Attempts Transiently Interfere with Concurrent Encoding of Episodic Memories But Not Vice Versa

Allan¹,

Allen²

2005

J. Neurosci.

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In the rodent hippocampus, different phases of each theta activity cycle may be devoted to encoding and retrieval processes. These cycles of ϳ3-8 Hz would allow equal processing time for each state and also provide temporal segregation to minimize their mutual interference. We show here that, by controlling the presentation asynchrony between verbal encoding and retrieval cues, theta-resolution (Ͻ100 ms) interference-free shifts between functional states are not expressed in hippocampally dependent, human "episodic" memory. Instead, retrieval attempts selectively and transiently interfere, for ϳ450 ms, with the encoding of ongoing experiences. Analyses of scalp event-related potentials confirmed that the functional state of the brain during retrieval is largely unperturbed by concurrent encoding and also suggested that encoding impairments may last until a neocortical phase of retrieval can begin. The findings reveal the dynamic properties of interdependent encoding and retrieval functions that contribute to episodic memory in vivo and, moreover, show that, in humans, this form of memory does not operate with either the equality, or the rapidity, intrinsic to the theta model of rodent hippocampal function.

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“…The two studies that showed significant effects of the hippocampal stimulation on memory encoding (at least p < .01; Coleshill et al, 2004 andLacruz et al, 2010) also did not show complete memory disruption (patients' performance were not consistently at chance levels across all stimulation trials). One explanation for these counterintuitive findings is that given that the hippocampus is a large structure, stimulation delivered to one part of it would not have striking effects on memory as hippocampal lesions do.…”

Section: Hypothalamic Stimulationmentioning

confidence: 93%

“…We discuss six aDES studies on memory modulation which provide a useful framework for considering the varying effects of hippocampal stimulation on memory performance (Coleshill et al, 2004;Fell et al, 2013;Koubeissi, Kahriman, Syed, Miller, & Durand, 2013;Lacruz et al, 2010;Miller et al, 2015;Suthana et al, 2012). These studies all used depth electrodes targeting the hippocampus, parahippocampal cortex, or fornix.…”

mentioning

confidence: 99%

A network approach for modulating memory processes via direct and indirect brain stimulation: Toward a causal approach for the neural basis of memory

Kim¹,

Ekstrom

Tandon³

2016

Neurobiology of Learning and Memory

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A network approach for modulating memory processes via direct and indirect brain stimulation: Toward a causal approach for the neural basis of memory This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. that disrupting frontal or parietal regions also impairs memory performance, suggesting that these regions also play necessary roles in declarative memory. On the other hand, a handful of both invasive and non-invasive studies have also suggested modest improvements in memory performance following stimulation. These studies typically target brain regions connected to the hippocampus or other memory "hubs," which may affect endogenous activity in connected areas like the hippocampus, suggesting that to augment declarative memory, altering the broader endogenous memory network activity is critical. Together, studies reporting memory improvements / impairments are consistent with the idea that a network of distinct brain "hubs" may be crucial for successful memory encoding and retrieval rather than a single primary hub such as the hippocampus. Thus, it is important to consider neurostimulation from the network perspective, rather than from a purely localizationalist viewpoint. We conclude by proposing a novel approach to neurostimulation for declarative memory modulation that aims to facilitate interactions between multiple brain "nodes" underlying memory rather than considering individual brain regions in isolation.

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Material-Specific Recognition Memory Deficits Elicited by Unilateral Hippocampal Electrical Stimulation

Cited by 120 publications

References 49 publications

Hippocampal Lesion Patterns in Acute Posterior Cerebral Artery Stroke

Hippocampal Lesion Patterns in Acute Posterior Cerebral Artery Stroke

Retrieval Attempts Transiently Interfere with Concurrent Encoding of Episodic Memories But Not Vice Versa

A network approach for modulating memory processes via direct and indirect brain stimulation: Toward a causal approach for the neural basis of memory

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