Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility?

Burke, John F.; Ramayya, Ashwin G.; Kahana, Michael J.

doi:10.1016/j.conb.2014.09.003

Cited by 94 publications

(126 citation statements)

References 47 publications

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“…Concretely, frequency bands below 30 Hz showed less power for CRs than Hits, with SPL channels showing the largest effect. This nontonal observation for low-frequency bands in ECoG data is commonly observed in the literature (52). Future research is needed to understand why the putative delta, theta, alpha, and beta bands, measured from left dorsal PPC, are not selectively involved in memory-guided decision making.…”

Section: Discussionmentioning

confidence: 68%

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Gonzalez

Hutchinson

Uncapher

et al. 2015

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

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Theories of the neurobiology of episodic memory predominantly focus on the contributions of medial temporal lobe structures, based on extensive lesion, electrophysiological, and imaging evidence. Against this backdrop, functional neuroimaging data have unexpectedly implicated left posterior parietal cortex (PPC) in episodic retrieval, revealing distinct activation patterns in PPC subregions as humans make memory-related decisions. To date, theorizing about the functional contributions of PPC has been hampered by the absence of information about the temporal dynamics of PPC activity as retrieval unfolds. Here, we leveraged electrocorticography to examine the temporal profile of high gamma power (HGP) in dorsal PPC subregions as participants made old/new recognition memory decisions. A double dissociation in memory-related HGP was observed, with activity in left intraparietal sulcus (IPS) and left superior parietal lobule (SPL) differing in time and sign for recognized old items (Hits) and correctly rejected novel items (CRs). Specifically, HGP in left IPS increased for Hits 300-700 ms poststimulus onset, and decayed to baseline ∼200 ms preresponse. By contrast, HGP in left SPL increased for CRs early after stimulus onset (200−300 ms) and late in the memory decision (from 700 ms to response). These memory-related effects were unique to left PPC, as they were not observed in right PPC. Finally, memory-related HGP in left IPS and SPL was sufficiently reliable to enable brain-based decoding of the participant's memory state at the single-trial level, using multivariate pattern classification. Collectively, these data provide insights into left PPC temporal dynamics as humans make recognition memory decisions.intracranial EEG | declarative memory | decision making | multivariate pattern analysis | ECoG T he ability to remember past events-episodic memory-is known to critically depend on medial temporal lobe (MTL) structures (1, 2) and their interaction with prefrontal cortex (3). Neuroimaging studies of humans making memory-based decisions, although advancing understanding of MTL and prefrontal mnemonic function (4-8), consistently and unexpectedly demonstrate that activity in left lateral posterior parietal cortex (PPC) also varies with episodic memory outcomes (9-14). In particular, functional MRI (fMRI) data reveal dissociable effects of memory on activity in left intraparietal sulcus (IPS), superior parietal lobule (SPL), and angular gyrus (AG), wherein activity tracks perceived memory strength, retrieval decision uncertainty, and episodic recollection, respectively (9-14). For example, during recognition memory decisions, activity in left lateral IPS is greater during higher confidence hits and monotonically decreases across lower confidence hits to lower confidence correct rejections (CRs) to higher confidence CRs (15-17). By contrast, activity in left SPL is greater during lower confidence recognition decisions (for both hits and correct rejections) relative to higher confidence decisions (11,16,17).Studies of ...

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Section: Discussionmentioning

confidence: 68%

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Gonzalez

Hutchinson

Uncapher

et al. 2015

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

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“…Theta-gamma PAC was first described as a correlate of exploratory behavior in rodents (Buzsaki, 2002; Colgin, 2013) and has since been extensively studied in humans using ECoG, e.g., (Kahana et al, 1999). 3 It currently is widely accepted that high-frequency activity, e.g., gamma oscillations and spike discharge, reflect local processing (Buzsaki and Wang, 2012; Nir et al, 2007) whereas phase-synchronous slower activity, i.e., in the theta, alpha, beta frequency ranges (nominally, 4–30 Hz), coordinates excitability over widely separated parts of the brain (Bahramisharif et al, 2013; Burke et al, 2015; Ekstrom and Watrous, 2014; Jensen et al, 2014; van der Meij et al, 2012). This coordinating mechanism selectively links appropriate sensory, motor, task control, and memory modules according to instantaneous behavioral requirements (Fries, 2005; Helfrich and Knight, 2016).…”

Section: Discussionmentioning

confidence: 99%

“…It is generally agreed that engagement of the extrinsic system predominantly suppresses alpha oscillations (Klimesch, 1999; Miller et al, 2007; Sederberg et al, 2003). Engagement of the intrinsic system has been variably reported as enhancing (Colgin, 2013) or suppressing (Burke et al, 2015; Crespo-García et al, 2016; Greenberg et al, 2015) theta oscillations. However, if these modulations (of either sign) are spontaneously coordinated across regions (i.e., in the task-free state), we may expect to observe spectrally specific spatial correspondences between BLP correlations and BOLD fMRI RSNs.…”

Section: Introductionmentioning

confidence: 99%

Frequency-specific electrophysiologic correlates of resting state fMRI networks

Hacker¹,

Snyder²,

Pahwa³

et al. 2017

NeuroImage

145

107

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Resting state functional MRI (R-fMRI) studies have shown that slow (< 0.1 Hz), intrinsic fluctuations of the blood oxygen level dependent (BOLD) signal are temporally correlated within hierarchically organized functional systems known as resting state networks (RSNs) (Doucet et al., 2011). Most broadly, this hierarchy exhibits a dichotomy between two opposed systems (Fox et al., 2005). One system engages with the environment and includes the visual, auditory, and sensorimotor (SMN) networks as well as the dorsal attention network (DAN), which controls spatial attention. The other system includes the default mode network (DMN) and the fronto-parietal control system (FPC), RSNs that instantiate episodic memory and executive control, respectively. Here, we test the hypothesis, based on the spectral specificity of electrophysiologic responses to perceptual vs. memory tasks (Klimesch, 1999; Pfurtscheller and Lopes da Silva, 1999), that these two large-scale neural systems also manifest frequency specificity in the resting state. We measured the spatial correspondence between electrocorticographic (ECoG) band-limited power (BLP) and R-fMRI correlation patterns in awake, resting, human subjects. Our results show that, while gamma BLP correspondence was common throughout the brain, theta (4–8 Hz) BLP correspondence was stronger in the DMN and FPC, whereas alpha (8–12 Hz) correspondence was stronger in the SMN and DAN. Thus, the human brain, at rest, exhibits frequency specific electrophysiology, respecting both the spectral structure of task responses and the hierarchical organization of RSNs.

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“…HFA can be thought of as an activation signal that measures the overall firing rate of many thousands of neurons at the mesoscopic level (30,31,49) and intracranial HFA recorded from a macroelectrode can be interpreted very similarly as multiunit activity recorded by a microelectrode, albeit on a different spatial scale. In a recent study of recognition memory, Wixted et al (29) demonstrated that hippocampal single-unit and multiunit recordings contain information pertaining to stimulus evidence (true target-lure status, irrespective of response choice).…”

Section: Discussionmentioning

confidence: 99%

“…Given that HFA is a spatiotemporally precise marker of neural ensemble activity (30,31), if hippocampal activity correlated with successful recognition performance at retrieval, then, depending on which theory is correct, it should correlate either with behavioral estimates of recollection only or with behavioral estimates of both recollection and familiarity. Seen through the lens of dual-process theories of recognition (12), hippocampal HFA should identify whether this structure uniquely supports recollection.…”

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confidence: 99%

The human hippocampus contributes to both the recollection and familiarity components of recognition memory

Merkow

Burke

Kahana

2015

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

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Despite a substantial body of work comprising theoretical modeling, the effects of medial temporal lobe lesions, and electrophysiological signal analysis, the role of the hippocampus in recognition memory remains controversial. In particular, it is not known whether the hippocampus exclusively supports recollection or both recollection and familiarity-the two latent cognitive processes theorized to underlie recognition memory. We studied recognition memory in a large group of patients undergoing intracranial electroencephalographic (iEEG) monitoring for epilepsy. By measuring high-frequency activity (HFA)-a signal associated with precise spatiotemporal properties-we show that hippocampal activity during recognition predicted recognition memory performance and tracked both recollection and familiarity. Through the lens of dual-process models, these results indicate that the hippocampus supports both the recollection and familiarity processes.hippocampus | recognition memory | recollection | familiarity | high-frequency activity R ecognition is one's ability to judge an item as previously encountered. Whereas it is well known that the hippocampus plays a crucial role in human recall memory, the role of the hippocampus in recognition memory remains surprisingly controversial (1-4). A number of studies have reported that bilateral hippocampal injury in humans causes impaired recall, whereas recognition remains intact (5). Others document the preservation of recognition in the setting of hippocampal lesioning in nonhuman primates (6) and rodents (7). On the other hand, a substantial literature describes combined recall and recognition deficits in a similarly injured group of patients (8) and animals (9, 10).Recognition is thought to rely on two processes: familiarity, wherein upon seeing a person's face, the rememberer has only a vague sense he has met the person before, and recollection, wherein the subject sees the person's face and vividly remembers details of the encounter (11,12). What role the hippocampus plays in supporting these processes remains the subject of considerable debate. Many memory researchers have proposed the discrepancy in the lesion data above derives from the fact that the hippocampus, which is well known to play a role in associative and relational memory (13), exclusively subserves recollection, whereas familiarity is supported by the extrahippocampal medial temporal lobe (MTL) (14). By this account, humans and animals are able to compensate for the loss of the hippocampus, and thus recollection, by relying on familiarity (15-18). A contrasting view holds that the hippocampus instead contributes to both recollection and familiarity, thus explaining why hippocampal damage is associated with severe impairment of both processes and consequently the overall recognition performance (4,8,19,20). Whether neural circuitry underlying familiarity and recollection lie within the hippocampus has also been extensively studied using functional MRI (fMRI) (21). Still, that many fMRI experiments show that ...

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Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility?

Cited by 94 publications

References 47 publications

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Electrocorticography reveals the temporal dynamics of posterior parietal cortical activity during recognition memory decisions

Frequency-specific electrophysiologic correlates of resting state fMRI networks

The human hippocampus contributes to both the recollection and familiarity components of recognition memory

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