Painful laser stimuli induce directed functional interactions within and between the human amygdala and hippocampus

Liu, C.C.; Shi, Christine; Franaszczuk, Piotr J.; Crone, Nathan E.; Schretlen, D.; Ohara, Shuichi; Lenz, Fred A.

doi:10.1016/j.neuroscience.2011.01.029

Cited by 20 publications

(23 citation statements)

References 68 publications

(101 reference statements)

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“…This baseline normalization approach was used to conduct the statistical comparisons between stimulus relevant and stimulus irrelevant cross-frequency couplings. Similar statistical approaches were also used in previous event-related analysis (Pfurtscheller, 1992; Gross et al, 2007; Korzeniewska et al, 2011; Liu et al, 2010, 2011c). …”

Section: Methodsmentioning

confidence: 99%

Cross-frequency coupling in deep brain structures upon processing the painful sensory inputs

et al. 2015

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Cross-frequency coupling has been shown to be functionally significant in cortical information processing, potentially serving as a mechanism for integrating functionally relevant regions in the brain. In this study, we evaluate the hypothesis that pain-related gamma oscillatory responses are coupled with low-frequency oscillations in the frontal lobe, amygdala and hippocampus, areas known to have roles in pain processing. We delivered painful laser pulses to random locations on the dorsal hand of five patients with uncontrolled epilepsy requiring depth electrode implantation for seizure monitoring. Two blocks of 40 laser stimulations were delivered to each subject and the pain-intensity was controlled at five in a 0–10 scale by adjusting the energy level of the laser pulses. Local-field-potentials (LFPs) were recorded through bilaterally implanted depth electrode contacts to study the oscillatory responses upon processing the painful laser stimulations. Our results show that painful laser stimulations enhanced low-gamma (LH, 40–70 Hz) and high-gamma (HG, 70–110 Hz) oscillatory responses in the amygdala and hippocampal regions on the right hemisphere and these gamma responses were significantly coupled with the phases of theta (4–7 Hz) and alpha (8–12 Hz) rhythms during pain processing. Given the roles of these deep brain structures in emotion, these findings suggest that the oscillatory responses in these regions may play a role in integrating the affective component of pain, which may contribute to our understanding of the mechanisms underlying the affective information processing in humans.

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Section: Methodsmentioning

confidence: 99%

Cross-frequency coupling in deep brain structures upon processing the painful sensory inputs

et al. 2015

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“…After conditioning, the CS+ evokes the conditioned response, which was initially evoked by the US but not by the CS+. Recordings from these structures during surgery for epilepsy demonstrate that the amygdala and Frontal lobe structures are activated and interact with each other during fear conditioning (Liu et al, 2010, 2011c,d, 2015a). …”

Section: Introductionmentioning

confidence: 99%

Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy

et al. 2017

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Imaging studies have described hemodynamic activity during fear conditioning protocols with stimulus trains in which a visual conditioned stimulus (CS+) is paired with an aversive unconditioned stimulus (US, painful laser pulse) while another visual stimulus is unpaired (CS−). We now test the hypothesis that CS Event-Related Spectral Perturbations (ERSPs) are related to ratings of CS Expectancy (likelihood of pairing with the US), Valence (unpleasantness) and Salience (ability to capture attention). ERSP windows in EEG were defined by both time after the CS and frequency, and showed increased oscillatory power (Event Related Synchronization, ERS) in the delta/theta Windows (0–8 Hz) and the gamma Window (30–55 Hz). Decreased oscillatory power (Event Related Desynchronization – ERD) was found in alpha (8–14 Hz) and beta Windows (14–30 Hz). The delta/theta ERS showed a differential effect of CS+ versus CS− at Prefrontal, Frontal and Midline Channels, while alpha and beta ERD were greater at Parietal and Occipital Channels early in the stimulus train. The gamma ERS Window increased from Habituation to Acquisition over a broad area from Frontal and occipital electrodes. The CS Valence and Salience were greater for CS+ than CS−, and were correlated with each other and with the ERD at overlapping Channels, particularly in the alpha Window. Expectancy and CS Skin Conductance Response were greater for CS+ than CS− and were correlated with ERSP at fewer Channels than Valence or Salience. These results suggest that alpha ERSP activity during fear conditioning reflects Valence and Salience of the CSs more than conditioning per se. The CS Valence and Salience were correlated with each other and with ERSP in the alpha Window more commonly than in other windows. Delta/theta ERSP differentiates between CS+ and CS− over a Midline Channel at which ERSP is correlated with Expectancy ratings. Although, both Expectancy and CS Skin Conductance Response (SCR) were correlated with ERSP this correlation occurred at fewer and different Channels than those for Valence or Salience. These results suggest that ERSP activity is related to Valence and Salience of the CSs more than to conditioning per se.

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“…These nuclei project upon the central nucleus of the amygdala which is an output structure important for the expression of fear (Davis, 1992; Sotres-Bayon et al, 2006; Rauch et al, 2006; Pare et al, 2004; Liu et al, 2011b). This is the indirect pathway through the human amygdala, while the direct pathway transmits signals evoked by the US directly to the central nucleus (Liu et al, 2011b). …”

Section: Introductionmentioning

confidence: 99%

Fear conditioning is associated with dynamic directed functional interactions between and within the human amygdala, hippocampus, and frontal lobe

et al. 2011

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The current model of fear conditioning suggests that it is mediated through modules involving the amygdala (AMY), hippocampus (HIP), and frontal lobe (FL). We now test the hypothesis that habituation and acquisition stages of a fear conditioning protocol are characterized by different event-related causal interactions (ERC) within and between these modules. The protocol employed the painful cutaneous laser as the unconditioned stimulus and ERC was estimated by analysis of local field potentials recorded through electrodes implanted for investigation of epilepsy. During the pre-stimulus interval of the habituation stage FL>AMY ERC interactions were common. For comparison, in the post-stimulus interval of the habituation stage only a subdivision of the FL (dorsal lateral prefrontal cortex, dlPFC) still exerted the FL>AMY ERC interaction (dlFC>AMY). For a further comparison, during the poststimulus interval of the acquisition stage the dlPFC>AMY interaction persisted and an AMY>FL interaction appeared. In addition to these ERC interactions between modules, the results also show ERC interactions within modules. During the post-stimulus interval HIP>HIP ERC interactions were more common during acquisition, and deep hippocampal contacts exerted causal interactions upon superficial contacts, possibly explained by connectivity between the perihippocampal gyrus and the hippocampus. During the prestimulus interval of the habituation stage AMY>AMY ERC interactions were commonly found, while interactions between the deep and superficial amygdala (indirect pathway) were independent of intervals and stages. These results suggest that the network subserving fear includes distributed or widespread modules, some of which are themselves `local networks'. ERC interactions between and within modules can be either static or change dynamically across intervals or stages of fear conditioning.

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Painful laser stimuli induce directed functional interactions within and between the human amygdala and hippocampus

Cited by 20 publications

References 68 publications

Cross-frequency coupling in deep brain structures upon processing the painful sensory inputs

Cross-frequency coupling in deep brain structures upon processing the painful sensory inputs

Oscillatory EEG activity induced by conditioning stimuli during fear conditioning reflects Salience and Valence of these stimuli more than Expectancy

Fear conditioning is associated with dynamic directed functional interactions between and within the human amygdala, hippocampus, and frontal lobe

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