Altered hierarchical auditory predictive processing after lesions to the orbitofrontal cortex

Abstract:

Orbitofrontal cortex (OFC) is classically linked to inhibitory control, emotion regulation, and reward processing. Recent perspectives propose that the OFC also generates predictions about perceptual events, actions, and their outcomes. We tested the role of the OFC in detecting violations of prediction at two levels of abstraction (i.e., hierarchical predictive processing) by studying the event-related potentials (ERPs) of patients with focal OFC lesions (n = 12) and healthy controls (n = 14) while they detected deviant sequences of tones in a local–global paradigm. The structural regularities of the tones were controlled at two hierarchical levels by rules defined at a local (i.e., between tones within sequences) and at a global (i.e., between sequences) level. In OFC patients, ERPs elicited by standard tones were unaffected at both local and global levels compared to controls. However, patients showed an attenuated mismatch negativity (MMN) and P3a to local prediction violation, as well as a diminished MMN followed by a delayed P3a to the combined local and global level prediction violation. The subsequent P3b component to conditions involving violations of prediction at the level of global rules was preserved in the OFC group. Comparable effects were absent in patients with lesions restricted to the lateral PFC, which lends a degree of anatomical specificity to the altered predictive processing resulting from OFC lesion. Overall, the altered magnitudes and time courses of MMN/P3a responses after lesions to the OFC indicate that the neural correlates of detection of auditory regularity violation are impacted at two hierarchical levels of rule abstraction.

Authors:

• Olgerta Asko

• Alejandro Omar Blenkmann

• Sabine Liliana Leske

• Maja Dyhre Foldal

• Anais Llorens

• Ingrid Funderud

• Torstein R Meling

• Robert T Knight

• Tor Endestad

• Anne-Kristin Solbakk

Date: 2024

DOI: https://doi.org/10.7554/eLife.86386

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Orbitofrontal cortex governs working memory for temporal order

abstract:

How do we think about time? Converging lesion and neuroimaging evidence indicates that orbitofrontal cortex (OFC) supports the encoding and retrieval of temporal context in long-term memory, which may contribute to confabulation in individuals with OFC damage. Here, we reveal that OFC damage diminishes working memory for temporal order, that is, the ability to disentangle the relative recency of events as they unfold. OFC lesions reduced working memory for temporal order but not spatial position, and individual deficits were commensurate with lesion size. Comparable effects were absent in patients with lesions restricted to lateral prefrontal cortex (PFC). Based on these findings, we propose that OFC supports understanding of the order of events. Well-documented behavioral changes in individuals with OFC damage may relate to impaired temporal-order understanding.

authors:

• Elizabeth L Johnson

• William K Chang

• Callum D Dewar

• Donna Sorensen

• Jack J Lin

• Anne-Kristin Solbakk

• Tor Endestad

• Pal G Larsson

• Jugoslav Ivanovic

• Torstein R Meling

• Donatella Scabini

• Robert T Knight

Date: 2022

DOI: https:// doi.org/10.1016/j.cub.2022.03.074.

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Preservation of Interference Effects in Working Memory After Orbitofrontal Damage

Abstract:

Orbitofrontal cortex (OFC) is implicated in multiple cognitive processes, including inhibitory control, context memory, recency judgment, and choice behavior. Despite an emerging understanding of the role of OFC in memory and executive control, its necessity for core working memory (WM) operations remains undefined. Here, we assessed the impact of OFC damage on interference effects in WM using a Recent Probes task based on the Sternberg item-recognition task (1966). Subjects were asked to memorize a set of letters and then indicate whether a probe letter was presented in a particular set. Four conditions were created according to the forthcoming response (“yes”/“no”) and the recency of the probe (presented in the previous trial set or not). We compared behavioral and electroencephalography (EEG) responses between healthy subjects (n = 14) and patients with bilateral OFC damage (n = 14). Both groups had the same recency pattern of slower reaction time (RT) when the probe was presented in the previous trial but not in the current one, reflecting the proactive interference (PI). The within-group electrophysiological results showed no condition difference during letter encoding and maintenance. In contrast, event-related potentials (ERPs) to probes showed distinct within-group condition effects, and condition by group effects. The response and recency effects for controls occurred within the same time window (300–500 ms after probe onset) and were observed in two distinct spatial groups including right centro-posterior and left frontal electrodes. Both clusters showed ERP differences elicited by the response effect, and one cluster was also sensitive to the recency manipulation. Condition differences for the OFC group involved two different clusters, encompassing only left hemisphere electrodes and occurring during two consecutive time windows (345–463 ms and 565–710 ms). Both clusters were sensitive to the response effect, but no recency effect was found despite the behavioral recency effect. Although the groups had different electrophysiological responses, the maintenance of letters in WM, the evaluation of the context of the probe, and the decision to accept or reject a probed letter were preserved in OFC patients. The results suggest that neural reorganization may contribute to intact recency judgment and response after OFC damage.

Authors:

• Anaïs Llorens

• Ingrid Funderud

• Alejandro O Blenkmann

• James Lubell

• Maja Foldal

• Sabine Leske

• Rene Huster

• Torstein R Meling

• Robert T Knight

• Anne-Kristin Solbakk

• Tor Endestad

Date: 2020

DOI: https://doi.org/10.3389/fnhum.2019.00445

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Auditory deviance detection in the human insula: An intracranial EEG study

Abstract:

The human insula is known to be involved in auditory processing, but knowledge about its precise functional role and the underlying electrophysiology is limited. To assess its role in automatic auditory deviance detection we analyzed the EEG high frequency activity (HFA; 75–145 Hz) and ERPs from 90 intracranial insular channels across 16 patients undergoing pre-surgical intracranial monitoring for epilepsy treatment. Subjects passively listened to a stream of standard and deviant tones differing in four physical dimensions: intensity, frequency, location or time. HFA responses to auditory stimuli were found in the short and long gyri, and the anterior, superior, and inferior segments of the circular sulcus of the insular cortex. Only a subset of channels in the inferior segment of the circular sulcus of the insula showed HFA deviance detection responses, i.e., a greater and longer latency response to specific deviants relative to standards. Auditory deviancy processing was also later in the insula when compared with the superior temporal cortex. ERP results were more widespread and supported the HFA insular findings. These results provide evidence that the human insula is engaged during auditory deviance detection.

Authors:

• Alejandro O Blenkmann

• Santiago Collavini

• James Lubell

• Anaïs Llorens

• Ingrid Funderud

• Jugoslav Ivanovic

• Pål G Larsson

• Torstein R Meling

• Tristan Bekinschtein

• Silvia Kochen

• Tor Endestad

• Robert T Knight

• Anne-Kristin Solbakk

Date: 2019

DOI: https://doi.org/10.1016/j.cortex.2019.09.002

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Lesions to the fronto-parietal network impact alpha-band phase synchrony and cognitive control

Abstract:

Long-range phase synchrony in the α-oscillation band (near 10 Hz) has been proposed to facilitate information integration across anatomically segregated regions. Which areas may top-down regulate such cross-regional integration is largely unknown. We previously found that the moment-to-moment strength of high-α band (10–12 Hz) phase synchrony co-varies with activity in a fronto-parietal (FP) network. This network is critical for adaptive cognitive control functions such as cognitive flexibility required during set-shifting. Using electroencephalography (EEG) in 23 patients with focal frontal lobe lesions (resected tumors), we tested the hypothesis that the FP network is necessary for modulation of high-α band phase synchrony. Global phase-synchrony was measured using an adaptation of the phase-locking value (PLV) in a sliding window procedure, which allowed for measurement of changes in EEG-based resting-state functional connectivity across time. As hypothesized, the temporal modulation (range and standard deviation) of high-α phase synchrony was reduced as a function of FP network lesion extent, mostly due to dorsolateral prefrontal cortex (dlPFC) lesions. Furthermore, patients with dlPFC lesions exhibited reduced cognitive flexibility as measured by the Trail-Making Test (set-shifting). Our findings provide evidence that the FP network is necessary for modulatory control of high-α band long-range phase synchrony, and linked to cognitive flexibility.

Authors:

• Sepideh Sadaghiani

• Pascasie L Dombert

• Marianne Løvstad

• Ingrid Funderud

• Torstein R Meling

• Tor Endestad

• Robert T Knight

• Anne-Kristin Solbakk

• Mark D’Esposito

Date: 2018

DOI: 10.1093/cercor/bhy296

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