Publications by authors named "Youssef Ezzyat"

19 Publications

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Probing Network Mechanisms of Brain Stimulation in the Mood Circuit.

Authors:
Youssef Ezzyat

Neuron 2020 09;107(5):770-771

Department of Psychology, Wesleyan University, 207 High Street, Middletown, CT 06459, USA. Electronic address:

Direct brain stimulation has diverse effects on network activity. In this issue of Neuron, Qiao et al. (2020) demonstrate a novel approach for using stimulation to characterize and modulate interactions between areas of the mood processing network.
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http://dx.doi.org/10.1016/j.neuron.2020.08.008DOI Listing
September 2020

Tonic Resting State Hubness Supports High Gamma Activity Defined Verbal Memory Encoding Network in Epilepsy.

Neuroscience 2020 01 28;425:194-216. Epub 2019 Nov 28.

Department of Neurology, Thomas Jefferson University, Philadelphia, PA 19107, United States. Electronic address:

High gamma activity (HGA) of verbal-memory encoding using invasive-electroencephalogram has laid the foundation for numerous studies testing the integrity of memory in diseased populations. Yet, the functional connectivity characteristics of networks subserving these memory linkages remains uncertain. By integrating this electrophysiological biomarker of memory encoding from IEEG with resting-state BOLD fluctuations, we estimated the segregation and hubness of HGA-memory regions in drug-resistant epilepsy patients and matched healthy controls. HGA-memory regions express distinctly different hubness compared to neighboring regions in health and in epilepsy, and this hubness was more relevant than segregation in predicting verbal memory encoding. The HGA-memory network comprised regions from both the cognitive control and primary processing networks, validating that effective verbal-memory encoding requires integrating brain functions, and is not dominated by a central cognitive core. Our results demonstrate a tonic intrinsic set of functional connectivity, which provides the necessary conditions for effective, phasic, task-dependent memory encoding.
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http://dx.doi.org/10.1016/j.neuroscience.2019.11.001DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6945984PMC
January 2020

Does data cleaning improve brain state classification?

J Neurosci Methods 2019 12 18;328:108421. Epub 2019 Sep 18.

Dept. of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address:

Background: Neuroscientists routinely seek to identify and remove noisy or artifactual observations from their data. They do so with the belief that removing such data improves power to detect relations between neural activity and behavior, which are often subtle and can be overwhelmed by noise. Whereas standard methods can exclude certain well-defined noise sources (e.g., 50/60 Hz electrical noise), in many situations there is not a clear difference between noise and signals so it is not obvious how to separate the two. Here we ask whether methods routinely used to "clean" human electrophysiological recordings lead to greater power to detect brain-behavior relations.

New Method: This, to the authors' knowledge, is the first large-scale simultaneous evaluation of multiple commonly used methods for removing noise from intracranial EEG recordings.

Results: We find that several commonly used data cleaning methods (automated methods based on statistical signal properties and manual methods based on expert review) do not increase the power to detect univariate and multivariate electrophysiological biomarkers of successful episodic memory encoding, a well-characterized broadband pattern of neural activity observed across the brain.

Comparison With Existing Methods: Researchers may be more likely to increase statistical power to detect physiological phenomena of interest by allocating resources away from cleaning noisy data and toward collecting more within-patient observations.

Conclusions: These findings highlight the challenge of partitioning signal and noise in the analysis of brain-behavior relations, and suggest increasing sample size and numbers of observations, rather than data cleaning, as the best approach to improving statistical power.
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http://dx.doi.org/10.1016/j.jneumeth.2019.108421DOI Listing
December 2019

Functional control of electrophysiological network architecture using direct neurostimulation in humans.

Netw Neurosci 2019 1;3(3):848-877. Epub 2019 Jul 1.

Department of Bioengineering, University of Pennsylvania, Philadelphia, PA, USA.

Chronically implantable neurostimulation devices are becoming a clinically viable option for treating patients with neurological disease and psychiatric disorders. Neurostimulation offers the ability to probe and manipulate distributed networks of interacting brain areas in dysfunctional circuits. Here, we use tools from network control theory to examine the dynamic reconfiguration of functionally interacting neuronal ensembles during targeted neurostimulation of cortical and subcortical brain structures. By integrating multimodal intracranial recordings and diffusion-weighted imaging from patients with drug-resistant epilepsy, we test hypothesized structural and functional rules that predict altered patterns of synchronized local field potentials. We demonstrate the ability to predictably reconfigure functional interactions depending on stimulation strength and location. Stimulation of areas with structurally weak connections largely modulates the functional hubness of downstream areas and concurrently propels the brain towards more difficult-to-reach dynamical states. By using focal perturbations to bridge large-scale structure, function, and markers of behavior, our findings suggest that stimulation may be tuned to influence different scales of network interactions driving cognition.
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http://dx.doi.org/10.1162/netn_a_00089DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6663306PMC
July 2019

Differentiation of Human Medial Prefrontal Cortex Activity Underlies Long-Term Resistance to Forgetting in Memory.

J Neurosci 2018 11 16;38(48):10244-10254. Epub 2018 Jul 16.

Department of Psychology, Columbia University, New York, New York 10027

It is well known that distributing study events over time leads to better memory over long time scales, compared with massing study events together. One explanation for such long-term resistance to forgetting is that distributed study leads to neural differentiation in memory, which supports retrieval of past experiences by disambiguating highly similar memory representations. Neuroanatomical models of episodic memory retrieval propose that the hippocampus and medial prefrontal cortex (MPFC) work together to enable retrieval of behaviorally appropriate memories. However, it is not known how representations in these regions jointly support resistance to forgetting long after initial learning. Using fMRI, we measured differentiation in retrieved memory representations following an extended delay in male and female human participants. After 1 week, word-object associations were better remembered if studied across 2 d (overnight), allowing associations to be learned in distinct temporal contexts, compared with learning within a single day (same day). MPFC retrieval patterns showed differentiation for overnight relative to same day memories, whereas hippocampal patterns reflected associative retrieval success. Overnight memory differentiation in MPFC was higher for associative than item memories and higher than differentiation assessed over a brain-wide set of retrieval-active voxels. The memory-related difference in MPFC pattern differentiation correlated with memory success for overnight learning and with hippocampal-MPFC functional connectivity. These results show that learning information across days leads to differentiated MPFC memory representations, reducing forgetting after 1 week, and suggest this arises from persistent interactions between MPFC and hippocampus. Neural activity in both the hippocampus and medial prefrontal cortex (MPFC) has been linked to memory-related representations, but prior work has not examined how these representations support episodic memory retrieval over extended time scales that are characteristic of everyday retrieval. We show that differentiation in MPFC activity 1 week after encoding is higher for retrieved information learned across 2 d compared with within a single day. In hippocampus, differentiation was greater for detailed memory retrieval but was not influenced by whether information had been learned over 1 or 2 d. Differentiation in MPFC predicted behavioral robustness to forgetting and was correlated with hippocampal-MPFC connectivity. The results suggest that context-based differentiation supports robust long-term memory via persistent MPFC-hippocampal interactions.
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http://dx.doi.org/10.1523/JNEUROSCI.2290-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6262147PMC
November 2018

Electrical Stimulation in Hippocampus and Entorhinal Cortex Impairs Spatial and Temporal Memory.

J Neurosci 2018 05 10;38(19):4471-4481. Epub 2018 Apr 10.

Department of Biomedical Engineering, Columbia University, New York, New York 10027,

The medial temporal lobe (MTL) is widely implicated in supporting episodic memory and navigation, but its precise functional role in organizing memory across time and space remains elusive. Here we examine the specific cognitive processes implemented by MTL structures (hippocampus and entorhinal cortex) to organize memory by using electrical brain stimulation, leveraging its ability to establish causal links between brain regions and features of behavior. We studied neurosurgical patients of both sexes who performed spatial-navigation and verbal-episodic memory tasks while brain stimulation was applied in various regions during learning. During the verbal memory task, stimulation in the MTL disrupted the temporal organization of encoded memories such that items learned with stimulation tended to be recalled in a more randomized order. During the spatial task, MTL stimulation impaired subjects' abilities to remember items located far away from boundaries. These stimulation effects were specific to the MTL. Our findings thus provide the first causal demonstration in humans of the specific memory processes that are performed by the MTL to encode when and where events occurred. Numerous studies have implicated the medial temporal lobe (MTL) in encoding spatial and temporal memories, but they have not been able to causally demonstrate the nature of the cognitive processes by which this occurs in real-time. Electrical brain stimulation is able to demonstrate causal links between a brain region and a given function with high temporal precision. By examining behavior in a memory task as subjects received MTL stimulation, we provide the first causal evidence demonstrating the role of the MTL in organizing the spatial and temporal aspects of episodic memory.
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http://dx.doi.org/10.1523/JNEUROSCI.3049-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5943975PMC
May 2018

Perceptual boundaries cause mnemonic trade-offs between local boundary processing and across-trial associative binding.

J Exp Psychol Learn Mem Cogn 2018 Jul 19;44(7):1075-1090. Epub 2018 Feb 19.

Department of Psychology, New York University.

Episodic memories are not veridical records of our lives, but rather are better described as organized summaries of experience. Theories and empirical research suggest that shifts in perceptual, temporal, and semantic information lead to a chunking of our continuous experiences into segments, or "events." However, the consequences of these contextual shifts on memory formation and organization remains unclear. In a series of 3 behavioral studies, we introduced context shifts (or "event boundaries") between trains of stimuli and then examined the influence of the boundaries on several measures of associative memory. In Experiment 1, we found that perceptual event boundaries strengthened associative binding of item-context pairings present at event boundaries. In Experiment 2, we observed reduced temporal order memory for items encoded in distinct events relative to items encoded within the same event, and a trade-off between the speed of processing at boundaries, and temporal order memory for items that flanked those boundaries. Finally, in Experiment 3 we found that event organization imprinted structure on the order in which items were freely recalled. These results provide insight into how boundary- and event-related organizational processes during encoding shape subsequent representations of events in episodic memory. (PsycINFO Database Record
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http://dx.doi.org/10.1037/xlm0000503DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6013306PMC
July 2018

Closed-loop stimulation of temporal cortex rescues functional networks and improves memory.

Nat Commun 2018 02 6;9(1):365. Epub 2018 Feb 6.

Department of Psychology, University of Pennsylvania, 433 South University Avenue, Philadelphia, PA, 19104, USA.

Memory failures are frustrating and often the result of ineffective encoding. One approach to improving memory outcomes is through direct modulation of brain activity with electrical stimulation. Previous efforts, however, have reported inconsistent effects when using open-loop stimulation and often target the hippocampus and medial temporal lobes. Here we use a closed-loop system to monitor and decode neural activity from direct brain recordings in humans. We apply targeted stimulation to lateral temporal cortex and report that this stimulation rescues periods of poor memory encoding. This system also improves later recall, revealing that the lateral temporal cortex is a reliable target for memory enhancement. Taken together, our results suggest that such systems may provide a therapeutic approach for treating memory dysfunction.
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http://dx.doi.org/10.1038/s41467-017-02753-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5802791PMC
February 2018

Electrical Stimulation Modulates High γ Activity and Human Memory Performance.

eNeuro 2018 Jan-Feb;5(1). Epub 2018 Feb 2.

Department of Neurology, Mayo Clinic, Rochester, MN 55905.

Direct electrical stimulation of the brain has emerged as a powerful treatment for multiple neurological diseases, and as a potential technique to enhance human cognition. Despite its application in a range of brain disorders, it remains unclear how stimulation of discrete brain areas affects memory performance and the underlying electrophysiological activities. Here, we investigated the effect of direct electrical stimulation in four brain regions known to support declarative memory: hippocampus (HP), parahippocampal region (PH) neocortex, prefrontal cortex (PF), and lateral temporal cortex (TC). Intracranial EEG recordings with stimulation were collected from 22 patients during performance of verbal memory tasks. We found that high γ (62-118 Hz) activity induced by word presentation was modulated by electrical stimulation. This modulatory effect was greatest for trials with "poor" memory encoding. The high γ modulation correlated with the behavioral effect of stimulation in a given brain region: it was negative, i.e., the induced high γ activity was decreased, in the regions where stimulation decreased memory performance, and positive in the lateral TC where memory enhancement was observed. Our results suggest that the effect of electrical stimulation on high γ activity induced by word presentation may be a useful biomarker for mapping memory networks and guiding therapeutic brain stimulation.
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http://dx.doi.org/10.1523/ENEURO.0369-17.2018DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5797477PMC
January 2019

Evidence for verbal memory enhancement with electrical brain stimulation in the lateral temporal cortex.

Brain 2018 04;141(4):971-978

Mayo Clinic, Department of Neurology, Rochester MN, USA.

Direct electrical stimulation of the human brain can elicit sensory and motor perceptions as well as recall of memories. Stimulating higher order association areas of the lateral temporal cortex in particular was reported to activate visual and auditory memory representations of past experiences (Penfield and Perot, 1963). We hypothesized that this effect could be used to modulate memory processing. Recent attempts at memory enhancement in the human brain have been focused on the hippocampus and other mesial temporal lobe structures, with a few reports of memory improvement in small studies of individual brain regions. Here, we investigated the effect of stimulation in four brain regions known to support declarative memory: hippocampus, parahippocampal neocortex, prefrontal cortex and temporal cortex. Intracranial electrode recordings with stimulation were used to assess verbal memory performance in a group of 22 patients (nine males). We show enhanced performance with electrical stimulation in the lateral temporal cortex (paired t-test, P = 0.0067), but not in the other brain regions tested. This selective enhancement was observed both on the group level, and for two of the four individual subjects stimulated in the temporal cortex. This study shows that electrical stimulation in specific brain areas can enhance verbal memory performance in humans.awx373media15704855796001.
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http://dx.doi.org/10.1093/brain/awx373DOI Listing
April 2018

Direct Brain Stimulation Modulates Encoding States and Memory Performance in Humans.

Curr Biol 2017 May 20;27(9):1251-1258. Epub 2017 Apr 20.

Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address:

People often forget information because they fail to effectively encode it. Here, we test the hypothesis that targeted electrical stimulation can modulate neural encoding states and subsequent memory outcomes. Using recordings from neurosurgical epilepsy patients with intracranially implanted electrodes, we trained multivariate classifiers to discriminate spectral activity during learning that predicted remembering from forgetting, then decoded neural activity in later sessions in which we applied stimulation during learning. Stimulation increased encoding-state estimates and recall if delivered when the classifier indicated low encoding efficiency but had the reverse effect if stimulation was delivered when the classifier indicated high encoding efficiency. Higher encoding-state estimates from stimulation were associated with greater evidence of neural activity linked to contextual memory encoding. In identifying the conditions under which stimulation modulates memory, the data suggest strategies for therapeutically treating memory dysfunction.
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http://dx.doi.org/10.1016/j.cub.2017.03.028DOI Listing
May 2017

Similar patterns of neural activity predict memory function during encoding and retrieval.

Neuroimage 2017 07 2;155:60-71. Epub 2017 Apr 2.

Department of Psychology, University of Pennsylvania, Philadelphia PA 19104, USA. Electronic address:

Neural networks that span the medial temporal lobe (MTL), prefrontal cortex, and posterior cortical regions are essential to episodic memory function in humans. Encoding and retrieval are supported by the engagement of both distinct neural pathways across the cortex and common structures within the medial temporal lobes. However, the degree to which memory performance can be determined by neural processing that is common to encoding and retrieval remains to be determined. To identify neural signatures of successful memory function, we administered a delayed free-recall task to 187 neurosurgical patients implanted with subdural or intraparenchymal depth electrodes. We developed multivariate classifiers to identify patterns of spectral power across the brain that independently predicted successful episodic encoding and retrieval. During encoding and retrieval, patterns of increased high frequency activity in prefrontal, MTL, and inferior parietal cortices, accompanied by widespread decreases in low frequency power across the brain predicted successful memory function. Using a cross-decoding approach, we demonstrate the ability to predict memory function across distinct phases of the free-recall task. Furthermore, we demonstrate that classifiers that combine information from both encoding and retrieval states can outperform task-independent models. These findings suggest that the engagement of a core memory network during either encoding or retrieval shapes the ability to remember the past, despite distinct neural interactions that facilitate encoding and retrieval.
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http://dx.doi.org/10.1016/j.neuroimage.2017.03.042DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5789770PMC
July 2017

Direct Electrical Stimulation of the Human Entorhinal Region and Hippocampus Impairs Memory.

Neuron 2016 Dec;92(5):983-990

Department of Psychology, University of Pennsylvania, Philadelphia, PA 19104, USA.

Deep brain stimulation (DBS) has shown promise for treating a range of brain disorders and neurological conditions. One recent study showed that DBS in the entorhinal region improved the accuracy of human spatial memory. Based on this line of work, we performed a series of experiments to more fully characterize the effects of DBS in the medial temporal lobe on human memory. Neurosurgical patients with implanted electrodes performed spatial and verbal-episodic memory tasks. During the encoding periods of both tasks, subjects received electrical stimulation at 50 Hz. In contrast to earlier work, electrical stimulation impaired memory performance significantly in both spatial and verbal tasks. Stimulation in both the entorhinal region and hippocampus caused decreased memory performance. These findings indicate that the entorhinal region and hippocampus are causally involved in human memory and suggest that refined methods are needed to use DBS in these regions to improve memory.
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http://dx.doi.org/10.1016/j.neuron.2016.10.062DOI Listing
December 2016

Episodic sequence memory is supported by a theta-gamma phase code.

Nat Neurosci 2016 10 29;19(10):1374-80. Epub 2016 Aug 29.

Department of Psychology, New York University, New York, New York, USA.

The meaning we derive from our experiences is not a simple static extraction of the elements but is largely based on the order in which those elements occur. Models propose that sequence encoding is supported by interactions between high- and low-frequency oscillations, such that elements within an experience are represented by neural cell assemblies firing at higher frequencies (gamma) and sequential order is encoded by the specific timing of firing with respect to a lower frequency oscillation (theta). During episodic sequence memory formation in humans, we provide evidence that items in different sequence positions exhibit greater gamma power along distinct phases of a theta oscillation. Furthermore, this segregation is related to successful temporal order memory. Our results provide compelling evidence that memory for order, a core component of an episodic memory, capitalizes on the ubiquitous physiological mechanism of theta-gamma phase-amplitude coupling.
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http://dx.doi.org/10.1038/nn.4374DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5039104PMC
October 2016

The end point of the ventral visual stream: face and non-face perceptual deficits following unilateral anterior temporal lobe damage.

Neurocase 2015 19;21(5):554-62. Epub 2014 Sep 19.

a Department of Psychology , Temple University , Philadelphia , PA , USA.

While it has been claimed that the ventral visual stream ends in the inferior aspects of the anterior temporal lobe (ATL), little is known about whether this region is important for visual perception. Here the performance of two patients with unilateral ATL damage was assessed across four visual perception tasks that parametrically varied stimulus similarity. Patients performed normally on difficult judgments of circle size or face age but were impaired on face identity and dot pattern matching tasks. Portions of the ATL, most likely the ventral surface, may have a functional role in visual perception tasks requiring detailed configural processing, most commonly used to discern facial identity.
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http://dx.doi.org/10.1080/13554794.2014.959025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4366355PMC
March 2016

Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity.

Neuron 2014 Mar;81(5):1179-1189

Department of Psychology, New York University, 6 Washington Place, New York, NY 10003, USA; Center for Neural Science, New York University, 4 Washington Place, New York, NY 10003, USA. Electronic address:

Experiences unfold over time, but little is known about the mechanisms that support the formation of coherent episodic memories for temporally extended events. Recent work in animals has provided evidence for signals in hippocampus that could link events across temporal gaps; however, it is unknown whether and how such signals might be related to later memory for temporal information in humans. We measured patterns of fMRI BOLD activity as people encoded items that were separated in time and manipulated the presence of shared or distinct context across items. We found that hippocampal pattern similarity in the BOLD response across trials predicted later temporal memory decisions when context changed. By contrast, pattern similarity in lateral occipital cortex was related to memory only when context remained stable. These data provide evidence in humans that representational stability in hippocampus across time may be a mechanism for temporal memory organization.
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http://dx.doi.org/10.1016/j.neuron.2014.01.042DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3983791PMC
March 2014

What constitutes an episode in episodic memory?

Psychol Sci 2011 Feb 22;22(2):243-52. Epub 2010 Dec 22.

Department of Psychology and Center for Neural Science, New York University, 6 Washington Place, Room 866B, New York, NY 10003, USA.

The idea of episodic memory implies the existence of a process that segments experience into episodes so that they can be stored in memory. It is therefore surprising that the link between event segmentation and the organization of experiences into episodes in memory has not been addressed. We found that after participants read narratives containing temporal event boundaries at varying locations in the narrative, their long-term associative memory for information across event boundaries was lower than their memory for information within an event. This suggests that event segmentation during encoding resulted in segmentation of those same events in memory. Further, functional imaging data revealed that, across participants, brain activity consistent with the ongoing integration of information within events correlated with this pattern of mnemonic segmentation. These data are the first to address the mechanisms that support the organization of experiences into episodes in long-term memory.
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http://dx.doi.org/10.1177/0956797610393742DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4451827PMC
February 2011

The medial temporal lobe and visual working memory: comparisons across tasks, delays, and visual similarity.

Cogn Affect Behav Neurosci 2008 Mar;8(1):32-40

University ofPennsylvania, Philadelphia, Pennsylvania, USA.

Whether the hippocampus and medial temporal lobe (MTL) play any important role in visual working memory is a relatively new and controversial research question. The primary goal of this study was to assess working memory for faces over very short delays in patients with MTL damage. Patients and matched controls were required to remember one face that was parametrically morphed to be more or less similar to a probe face, over either a 1- or an 8-sec delay. Memory was assessed using both forced choice and old-new recognition tasks. The results show that MTL damage impairs both speed and accuracy of visual working memory across tasks. We speculate that the hippocampus is generally necessary for memory encoding.
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http://dx.doi.org/10.3758/cabn.8.1.32DOI Listing
March 2008

The Enigmatic temporal pole: a review of findings on social and emotional processing.

Brain 2007 Jul 28;130(Pt 7):1718-31. Epub 2007 Mar 28.

Center for Cognitive Neuroscience, University of Pennsylvania, 3720 Walnut Street, Room B51, Philadelphia, PA 19104-6196, USA.

The function of the anterior-most portion of the temporal lobes, the temporal pole, is not well understood. Anatomists have long considered it part of an extended limbic system based on its location posterior to the orbital frontal cortex and lateral to the amygdala, along with its tight connectivity to limbic and paralimbic regions. Here we review the literature in both non-human primates and humans to assess the temporal pole's putative role in social and emotional processing. Reviewed findings indicate that it has some role in both social and emotional processes, including face recognition and theory of mind, that goes beyond semantic memory. We propose that the temporal pole binds complex, highly processed perceptual inputs to visceral emotional responses. Because perceptual inputs remain segregated into dorsal (auditory), medial (olfactory) and ventral (visual) streams, the integration of emotion with perception is channel specific.
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http://dx.doi.org/10.1093/brain/awm052DOI Listing
July 2007