Comparison of fMRI correlates of successful episodic memory encoding in temporal lobe epilepsy patients and healthy controls

Hill, Paul F.; King, Danielle R.; Lega, Bradley; Rugg, Michael D.

doi:10.1016/j.neuroimage.2019.116397

Cited by 20 publications

(31 citation statements)

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“…Experimental applications of iEEG are currently limited to patients with medically refractory epilepsy, introducing potential constraints on the generalizability of intra-cerebral findings. Leveraging the noninvasiveness afforded by fMRI, we recently reported that group level BOLD SMEs in the same TLE patient cohort reported here did not reliably differ from SMEs observed in an age-matched neurologically healthy control group (Hill et al, 2020). Thus, neuropathology associated with TLE was apparently insufficient to give rise to detectable differences in the functional neuroanatomy of episodic memory encoding as this is reflected by the fMRI BOLD signal.…”

Section: Discussionmentioning

confidence: 55%

“…A separate single-trial GLM was constructed for each participant. Note that group level effects were reported previously by Hill et al (2020) and are beyond the scope of the current paper. Data from the six study sessions were concatenated and subjected to a ‘least-squares-all’ GLM (Mumford et al, 2014; Rissman et al, 2004) to estimate the BOLD response for each trial separately.…”

Section: Methodsmentioning

confidence: 72%

“…In the present study, 15 patients with medically resistant temporal lobe epilepsy (TLE) implanted with depth electrodes performed a verbal delayed free recall task while iEEG was recorded simultaneously from hippocampal and neocortical sites. The same patients subsequently performed a similar version of the free recall task in a later fMRI session (Hill et al, 2020). Subsequent memory effects (SMEs) were computed for fMRI and iEEG as patterns of encoding-related brain activity that were predictive of successful recall following a brief distractor interval (Paller & Wagner, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Distinct neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex

Hill¹,

Seger

Yoo

et al. 2021

Preprint

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Functional magnetic resonance imaging (fMRI) is among the foremost methods for mapping human brain function but provides only an indirect measure of underlying neural activity. Recent findings suggest that the neurophysiological correlates of the fMRI blood-oxygen-level-dependent (BOLD) signal might be regionally specific. We examined the neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex, where differences in neural architecture might result in a different relationship between the respective signals. Fifteen human neurosurgical patients (10 female, 5 male) implanted with depth electrodes performed a verbal free recall task while electrophysiological activity was recorded simultaneously from hippocampal and neocortical sites. The same patients subsequently performed a similar version of the task during a later fMRI session. Subsequent memory effects (SMEs) were computed for both imaging modalities as patterns of encoding-related brain activity predictive of later free recall. Linear mixed-effects modelling revealed that the relationship between BOLD and gamma-band SMEs was moderated by the lobar location of the recording site. BOLD and high gamma (70-150 Hz) SMEs positively covaried across much of the neocortex. This relationship was reversed in the hippocampus, where a negative correlation between BOLD and high gamma SMEs was evident. We also observed a negative relationship between BOLD and low gamma (30-70 Hz) SMEs in the medial temporal lobe more broadly. These results suggest that the neurophysiological correlates of the BOLD signal in the hippocampus differ from those observed in the neocortex.Significance StatementThe blood-oxygen-level-dependent (BOLD) signal forms the basis of fMRI but provides only an indirect measure of neural activity. Task-related modulation of BOLD signals are typically equated with changes in gamma-band activity; however, relevant empirical evidence comes largely from the neocortex. We examined neurophysiological correlates of the BOLD signal in the hippocampus, where the differing neural architecture might result in a different relationship between the respective signals. We identified a positive relationship between encoding-related changes in BOLD and gamma-band activity in frontal, temporal, and parietal cortex. This effect was reversed in the hippocampus, where BOLD and gamma-band effects negatively covaried. These results suggest regional variability in the transfer function between neural activity and the BOLD signal in the hippocampus and neocortex.

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Section: Discussionmentioning

confidence: 55%

Section: Methodsmentioning

confidence: 72%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Distinct neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex

Hill¹,

Seger

Yoo

et al. 2021

Preprint

Self Cite

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“…Previous studies have also shown that similar ERPs, characterized by latency, morphology, and amplitudes, are found across independent studies and epilepsy centers (e.g., Trautner et al 2004 vs. Barbeau et al 2008). Interestingly, a recent study combining iEEG and fMRI demonstrated only small functional neuroanatomical differences during an episodic memory task between a group of epileptic patients and a group of matched healthy subjects (Hill et al, 2020). Overall, despite the limitations, iEEG studies appear to provide useful and reliable information.…”

Section: Discussionmentioning

confidence: 99%

Dynamic connectivity analyses of intracranial EEG during recognition memory reveal various large-scale functional networks

Kopál

Hlinka

Despouy

et al. 2020

Preprint

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Recognition memory is the ability to recognize previously encountered events, objects, or people. It is characterized by its robustness and rapidness. Even this relatively simple ability requires the coordinated activity of a surprisingly large number of brain regions. These spatially distributed, but functionally linked regions are interconnected into large-scale networks. Understanding memory requires an examination of the involvement of these networks and the interactions between different regions while memory processes unfold. However, little is known about the dynamical organization of large-scale networks during the early phases of recognition memory. We recorded intracranial EEG, which affords high temporal and spatial resolution, while epileptic subjects performed a visual recognition memory task. We analyzed dynamic functional and effective connectivity as well as network properties. Various networks were identified, each with its specific characteristics regarding information flow (feedforward or feedback), dynamics, topology, and stability. The first network mainly involved the right visual ventral stream and bilateral frontal regions. It was characterized by early predominant feedforward activity, modular topology, and high stability. It was followed by the involvement of a second network, mainly in the left hemisphere, but notably also involving the right hippocampus, characterized by later feedback activity, integrated topology, and lower stability. The transition between networks was associated with a change in network topology. Overall, these results confirm that several large-scale brain networks, each with specific properties and temporal manifestation, are involved during recognition memory. Ultimately, understanding how the brain dynamically faces rapid changes in cognitive demand is vital to our comprehension of the neural basis of cognition.

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“…[Such "negative transfer" accounts were originally advanced to explain negative cortical and hippocampal post-stimulus SMEs (e.g., Otten and Rugg, 2001;Shrager et al, 2008;Staresina & Davachi, 2008;Hill et al, 2020]. From this perspective, therefore, the present negative prestimulus SMEs reflect the deleterious consequences of the successful encoding of study information incompatible with, or inaccessible to, the subsequent memory test.…”

Section: Negative Pre-stimulus Smesmentioning

confidence: 99%

Effects of age on pre-stimulus neural activity predictive of successful memory encoding: an fMRI study

Liu¹,

Koen

Rugg³

2020

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Pre-stimulus subsequent memory effects (SMEs) -differences in neural activity preceding the onset of study items that are predictive of later memory performance -have consistently been reported in young adults. The present fMRI experiment investigated potential age-related differences in pre-stimulus SMEs. During study, healthy young and older participants made one of two semantic judgments on images, with the judgment signaled by a preceding cue. In the test phase, participants first made an item recognition judgment and, for each item judged old, a source memory judgment. Age-invariant pre-stimulus SMEs were observed in left dorsomedial prefrontal cortex, left hippocampus, and right subgenual cortex. In each case, the effects reflected lower BOLD signal for later recognized items, regardless of source accuracy, than unrecognized items.A similar age-invariant pattern was observed in left orbitofrontal cortex, but the effect in this region was specific to items attracting a correct source response compared to unrecognized items. In contrast, the left angular gyrus and fusiform cortex demonstrated negative pre-stimulus SMEs that were exclusive to young participants. The findings indicate that age differences in pre-stimulus SMEs are regionally specific and suggest that pre-stimulus SMEs reflect multiple cognitive processes, only some of which are vulnerable to advancing age.

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Comparison of fMRI correlates of successful episodic memory encoding in temporal lobe epilepsy patients and healthy controls

Cited by 20 publications

References 53 publications

Distinct neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex

Distinct neurophysiological correlates of the fMRI BOLD signal in the hippocampus and neocortex

Dynamic connectivity analyses of intracranial EEG during recognition memory reveal various large-scale functional networks

Effects of age on pre-stimulus neural activity predictive of successful memory encoding: an fMRI study

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