Distinct iEEG activity patterns in temporal-limbic and prefrontal sites induced by emotional intentionality

Neomi Singer; Ilana Podlipsky; Fabrizio Esposito; Hadas Okon-Singer; Fani Andelman; Svetlana Kipervasser; Miri Y. Neufeld; Rainer Goebel; Itzhak Fried; Talma Hendler

doi:10.1016/j.cortex.2014.07.021

Distinct iEEG activity patterns in temporal-limbic and prefrontal sites induced by emotional intentionality

Neomi Singer, Ilana Podlipsky, Fabrizio Esposito, Hadas Okon-Singer, Fani Andelman, Svetlana Kipervasser, Miri Y. Neufeld, Rainer Goebel, Itzhak Fried, Talma Hendler

Research output: Contribution to journal › Article › peer-review

Abstract

Our emotions tend to be directed towards someone or something. Such emotional intentionality calls for the integration between two streams of information; abstract hedonic value and its associated concrete content. In a previous functional magnetic resonance imaging (fMRI) study we found that the combination of these two streams, as modeled by short emotional music excerpts and neutral film clips, was associated with synergistic activation in both temporal-limbic (TL) and ventral-lateral PFC (vLPFC) regions. This additive effect implies the integration of domain-specific 'affective' and 'cognitive' processes. Yet, the low temporal resolution of the fMRI limits the characterization of such cross-domain integration. To this end, we complemented the fMRI data with intracranial electroencephalogram (iEEG) recordings from twelve patients with intractable epilepsy. As expected, the additive fMRI activation in the amygdala and vLPFC was associated with distinct spatio-temporal iEEG patterns among electrodes situated within the vicinity of the fMRI activation foci. On the one hand, TL channels exhibited a transient (0-500msec) increase in gamma power (61-69Hz), possibly reflecting initial relevance detection or hedonic value tagging. On the other hand, vLPFC channels showed sustained (1-12sec) suppression of low frequency power (2.3-24Hz), possibly mediating changes in gating, enabling an on-going readiness for content-based processing of emotionally tagged signals. Moreover, an additive effect in delta-gamma phase-amplitude coupling (PAC) was found among the TL channels, possibly reflecting the integration between distinct domain specific processes. Together, this study provides a multi-faceted neurophysiological signature for computations that possibly underlie emotional intentionality in humans.

Original language	English
Pages (from-to)	121-138
Number of pages	18
Journal	Cortex
Volume	60
DOIs	https://doi.org/10.1016/j.cortex.2014.07.021
State	Published - 1 Nov 2014
Externally published	Yes

Bibliographical note

Funding Information:
The authors would like to thank the patients for their kind cooperation in participating in this study. We also thank Dr. Keren Rosenberg, Dr. Donna Abecasis, Dr. Irit Lichter-Shapira and Gadi Gilam for their assistance with the iEEG recordings; Andrey Zhdanov and Shahar Jamshy for their contribution to data analysis; Dr. Mordekhay Medvedovsky for his assistance in data assessment; David Yossef, Sari Nagar, Rivi Cohen, and the technicians at the EEG lab,Sourasky Medical Center for technical assistance; Dr. Roee Admon and Aliya Solski for their useful comments; Dr. Eran Eldar and Dr. Ori Ganor for providing the paradigm. This work was supported by the Israeli Science Foundation converging technologies grant ( ISF-1747/07 ) to T.H and I.F, by the EU ACTIVE grant ( FP7-ICT-2009-270460 ) to T.H and by scholarships from the Israeli Council for Higher Education (converging technologies) and Levie-Edersheim-Gitter Institute for Functional Brain Mapping and Israeli Science Foundation converging technologies fellowship to N.S.

Publisher Copyright:
© 2014 Elsevier Ltd.

Keywords

Emotional dynamics
Gamma power
High- and low frequency oscillations
IEEG and fMRI
Phase-amplitude-coupling

ASJC Scopus subject areas

Neuropsychology and Physiological Psychology
Experimental and Cognitive Psychology
Cognitive Neuroscience

Access to Document

10.1016/j.cortex.2014.07.021

Cite this

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title = "Distinct iEEG activity patterns in temporal-limbic and prefrontal sites induced by emotional intentionality",

abstract = "Our emotions tend to be directed towards someone or something. Such emotional intentionality calls for the integration between two streams of information; abstract hedonic value and its associated concrete content. In a previous functional magnetic resonance imaging (fMRI) study we found that the combination of these two streams, as modeled by short emotional music excerpts and neutral film clips, was associated with synergistic activation in both temporal-limbic (TL) and ventral-lateral PFC (vLPFC) regions. This additive effect implies the integration of domain-specific 'affective' and 'cognitive' processes. Yet, the low temporal resolution of the fMRI limits the characterization of such cross-domain integration. To this end, we complemented the fMRI data with intracranial electroencephalogram (iEEG) recordings from twelve patients with intractable epilepsy. As expected, the additive fMRI activation in the amygdala and vLPFC was associated with distinct spatio-temporal iEEG patterns among electrodes situated within the vicinity of the fMRI activation foci. On the one hand, TL channels exhibited a transient (0-500msec) increase in gamma power (61-69Hz), possibly reflecting initial relevance detection or hedonic value tagging. On the other hand, vLPFC channels showed sustained (1-12sec) suppression of low frequency power (2.3-24Hz), possibly mediating changes in gating, enabling an on-going readiness for content-based processing of emotionally tagged signals. Moreover, an additive effect in delta-gamma phase-amplitude coupling (PAC) was found among the TL channels, possibly reflecting the integration between distinct domain specific processes. Together, this study provides a multi-faceted neurophysiological signature for computations that possibly underlie emotional intentionality in humans.",

keywords = "Emotional dynamics, Gamma power, High- and low frequency oscillations, IEEG and fMRI, Phase-amplitude-coupling",

author = "Neomi Singer and Ilana Podlipsky and Fabrizio Esposito and Hadas Okon-Singer and Fani Andelman and Svetlana Kipervasser and Neufeld, {Miri Y.} and Rainer Goebel and Itzhak Fried and Talma Hendler",

note = "Funding Information: The authors would like to thank the patients for their kind cooperation in participating in this study. We also thank Dr. Keren Rosenberg, Dr. Donna Abecasis, Dr. Irit Lichter-Shapira and Gadi Gilam for their assistance with the iEEG recordings; Andrey Zhdanov and Shahar Jamshy for their contribution to data analysis; Dr. Mordekhay Medvedovsky for his assistance in data assessment; David Yossef, Sari Nagar, Rivi Cohen, and the technicians at the EEG lab,Sourasky Medical Center for technical assistance; Dr. Roee Admon and Aliya Solski for their useful comments; Dr. Eran Eldar and Dr. Ori Ganor for providing the paradigm. This work was supported by the Israeli Science Foundation converging technologies grant ( ISF-1747/07 ) to T.H and I.F, by the EU ACTIVE grant ( FP7-ICT-2009-270460 ) to T.H and by scholarships from the Israeli Council for Higher Education (converging technologies) and Levie-Edersheim-Gitter Institute for Functional Brain Mapping and Israeli Science Foundation converging technologies fellowship to N.S. Publisher Copyright: {\textcopyright} 2014 Elsevier Ltd.",

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AU - Andelman, Fani

AU - Kipervasser, Svetlana

AU - Neufeld, Miri Y.

AU - Goebel, Rainer

AU - Fried, Itzhak

AU - Hendler, Talma

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Distinct iEEG activity patterns in temporal-limbic and prefrontal sites induced by emotional intentionality

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

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