Amygdala lesion in temporal lobe epilepsy subjects impairs associative learning of emotional facial expressions

doi:10.1016/S0028-3932(00)00117-2

Neuropsychologia

Volume 39, Issue 3, 2001, Pages 231-236

https://doi.org/10.1016/S0028-3932(00)00117-2 Get rights and content

Abstract

To investigate the role of unilateral amygdala lesions on processing emotions, 22 drug-resistant temporal lobe epilepsy (TLE) subjects (12 with left-sided and ten with right-sided focus) were tested, after anterior temporal lobectomy or selective amygdalo-hippocampectomy on two associative learning tasks containing emotional and neutral facial expressions, respectively. Volumetric lesion analysis was performed on the basis of 3-D MR images. No effects of lesion side were found in TLE subjects. Taken the extent of amygdala damage into account, an interaction effect could be shown between task (learning of neutral facial expressions versus emotional facial expressions) and group (subjects with little versus considerable amygdala damage), indicating worse performance of subjects with considerable amygdala damage in learning emotional facial expressions. Subjects with considerable amygdala damage were also significantly impaired in learning emotional facial expressions when compared with control subjects.

Introduction

Looking for an anatomical correlate of emotion, animal research has pointed to the amygdala as a core structure [16]. The probably best known phenomenon of bilateral amygdala damage in non-human primates is the so-called ‘Klüver-Bucy syndrome’, producing an extraordinary loss of affective and social behaviour [28]. Anatomical studies have shown that the amygdala has numerous cortical and subcortical connections, receiving extensive convergent sensory input, and projecting it back not only upon unimodal, but also to association areas of the cortex, back-projections being most impressive for the visual system. The consequences of its bilateral destruction are discussed both as a disconnection syndrome, and as a disruption in forming stimulus-reward associations [2].

In humans, selective bilateral amygdala damage is extremely rare, and studies mostly rely on single cases. It does not seem to produce the same serious consequences as in non-human primates, but may disturb conditioning of autonomic responses [5], impair memory for emotional material [8], impair auditory recognition of fear and anger [21], and modulate social and emotional behaviour [25]. A number of studies, concentrating on the recognition of emotional facial expressions in humans with bilateral amygdala damage, have also found deficits, especially in recognising fear (e.g. [1], [9]). Thus, bilateral damage to the amygdala in humans may affect processing of emotional stimuli of different sensory qualities.

Unilateral amygdala damage is more common than bilateral amygdala damage in humans, but studies on its consequences regarding processing of emotions are less frequent. Electrophysiological studies on temporal lobe epilepsy subjects with implanted electrodes showed signals from the amygdala, when subjects reported affective experiences evoked by seizure discharge or electrical stimulation [13]. Single case studies with restricted unilateral amygdala damage indicated an impairment in processing emotional material [4], [29]. While studies based on amygdala-damaged subjects with additional damage to related cortical and subcortical regions found impaired fear conditioning [15], they failed to find an impairment in processing emotional facial expressions [1].

Taken together, there is strong evidence that bilateral amygdala damage in humans has consequences on processing emotional stimuli, while the effect of unilateral amygdala damage on emotion processing is less clear. Taking functional studies (PET, fMRI) with healthy subjects into account, both bilateral [7], and unilateral [18] amygdala activation could be found, while subjects were processing emotional stimuli.

The aim of the present study was to examine the influence of unilateral amygdala damage on the processing of emotional facial expressions as opposed to neutral facial expressions. Since the amygdala is closely related to mnemonic functions [2], [17], and also so far, there are no studies on amygdala damage and memory for emotional facial expressions, two associative learning tasks with emotional and neutral facial expressions were applied. We expected that subjects with major amygdala damage should show deficits in learning associations between emotional facial expressions compared with subjects with minor amygdala damage and control subjects, and compared with the learning of associations of between facial identities.

Section snippets

Subjects

Twenty-two subjects (12 females, ten males) with drug-resistant TLE, having undergone epilepsy surgery at the neurosurgical department of the University of Göttingen (between 1995 and 1997), were evaluated postsurgically (see Table 1). At time of testing, all subjects were on anticonvulsant medication. Pre- and postsurgical medication remained unchanged. Twelve subjects had been operated on the left temporal lobe, and ten on the right temporal lobe. Six subjects underwent selective

Results

Statistical comparisons showed that groups TLE-A and TLE-a did not differ significantly with respect to any sociodemographic, clinical, or neuropsychological variable. No significant differences were found comparing group performance in recognition of faces (BFRT), or in rating emotional facial expressions by valence and arousal. Both groups scored significantly lower in verbal memory functions and in TMT, Part A compared with control subjects. Performance on visual memory functions of TLE-A

Discussion

As predicted subjects with large lesions of the amygdala (TLE-A) scored lower in the Emotion Learning Task than subjects with only little damage to the amygdala (TLE-a) and control subjects (CG). No significant difference between TLE-a and the control group could be found in the Identity nor the Emotion Learning Task. Taken these findings together, our data indicate a relation between unilateral amygdala damage and impairment in the associative learning of emotional facial expressions.

This

Acknowledgements

The authors thank all the participating subjects, J. Baudewig for technical advice in performing 3d-MR images, and C. Saade, A. Kayser, and B. Goßler for performance of neuropsychological testing. Research was supported by grant Ir 15/6 of the Deutsche Forschungsgemeinschaft.

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Aberrant processing of emotional information has been reported in patients with affective disorders such as bipolar disorder and major depression [47]. Moreover, patients with TLE show selective associative learning impairment for emotional facial expressions, while patients with FLE exhibit associative learning problems for both emotional and neutral faces [48]. A possible explanation of the formers' difficulties might be given by their impaired amygdalar function, a critical structure in emotional processing, and/or the pathogenesis of depression.
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Decision making is essential in everyday life. Though the importance of the mesial temporal lobe in emotional processing and feedback learning is generally recognized, decision making in mesial temporal lobe epilepsy (mTLE) is almost unexplored so far. Twenty-eight consecutive epilepsy patients with drug resistant mTLE and fifty healthy controls performed decision tasks under initial ambiguity (participants have to learn by feedback to make advantageous decisions) and under risk (advantageous choices may be made by estimating risks and by rational strategies). A subgroup analysis compared the performance of patients affected by MRI-verified abnormalities of the hippocampus or amygdala. The effect of lesion side was also assessed. In decision under ambiguity, mTLE patients showed marked deficits and did not improve over the task. Patients with hippocampus abnormality and patients with amygdala abnormality showed comparable deficits. No difference was found between right and left TLE groups. In decision under risk, mTLE patients performed at the same level as controls. Results suggest that mTLE patients have difficulties in learning from feedback and in making decisions in uncertain, ambiguous situations. By contrast, they are able to make advantageous decisions when full information is given and risks, possible gains and losses are exactly defined.
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As observed by these authors [15], patients with FLE were impaired in associative learning for both emotional facial expressions and neutral faces. Instead, patients with TLE showed a more selective impairment for associative learning of emotional facial expressions, probably because of the damage to structures, such as the amygdala, that control the processing of emotional information [48]. The more global impairment of patients with FLE can be attributed to the long-lasting effects of frontal seizures (e.g., widespread inter- and intra-hemispheric propagation).
Frontal lobe epilepsy (FLE) is a seizure disorder with a lower prevalence than temporal lobe epilepsy (TLE). Despite its consequences on cognitive and emotional well-being, the neuropsychology of FLE has not been well studied. By contrast, TLE has been studied meticulously, leading to a relevant understanding of memory and the functional characteristics of the temporal and limbic circuits. The neuropsychological studies on FLE report deficits in motor coordination and planning, reduced attention span, and difficulties in response inhibition in complex cognitive tasks. This review aims to illustrate the most relevant neurocognitive dimensions, psychiatric comorbidity, and postoperative neuropsychological outcome of FLE. Methodological suggestions for future research are also included by critically reviewing the existing literature.
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Together with evidence against glial cell loss in the amygdala of BD (58), the remarkable degree of volume and neuron number reduction in the LN suggests that several subpopulations of neurons, possibly including projection neurons, may be affected in this disease. The LN is thought to play a major role in assigning emotional significance to external stimuli (2,59–63). The ABN is reciprocally connected to the LN and sends extensive projections to cortical and subcortical targets (e.g., 64,65–68).
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Total number and numeric density of neurons, neuronal somata size, and volume of the lateral (LN), basal (BN), accessory basal (ABN), and cortical (CO) nuclei of the amygdala were measured in 12 normal control, 10 BD, and 16 SZ subjects.
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Amygdala lesion in temporal lobe epilepsy subjects impairs associative learning of emotional facial expressions

Abstract

Introduction

Section snippets

Subjects

Results

Discussion

Acknowledgements

Trends in Neuroscience

Journal of Statistical Planning and Inference

Neuron

Brain and Cognition

Current Opinion in Neurobiology

Brain and Cognition

Neuroscience

Neuropsychologia

Fear and the human amygdala

The Journal of Neuroscience

Startle reflex and emotion modulation impairment after a right amygdala lesion

Brain

Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans

Science

The role of the right hemisphere in emotional communication

Brain

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Nature

Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear

Cognitive Neuropsychology