Edited by: Gernot Horstmann, Bielefeld University, Germany
Reviewed by: Elley Wakui, University of East London, United Kingdom; Xunbing Shen, Jiangxi University of Traditional Chinese Medicine, China
This article was submitted to Cognition, a section of the journal Frontiers in Psychology
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Lesion studies have shown that the right temporal lobe is crucial for recognition of facial expressions, particularly fear expressions. However, in previous studies, premorbid abilities of the patients were unknown and the effects of epileptic discharge could not be excluded. Herein, we report a case of a patient who underwent assessments of facial recognition before and after brain surgery and exhibited biased recognition of facial expressions. The patient was a 29-year-old right-handed male who underwent an awake craniotomy. Compared with the preoperative assessment, after the surgery, he showed biased recognition of surprised facial expressions, and his ability to recognize other facial expressions either improved or remained unchanged. These findings support the idea that the right temporal lobe is crucial for the recognition of facial expressions of surprise and that functional connectivity between various brain regions plays an important role in the ability to recognize facial expressions.
Functional imaging studies (e.g.,
The patient was a 29-year-old, right-handed male. Following graduation from graduate school, he worked as an office worker for 5 years. After experiencing olfactory hallucinations, he visited a local hospital and was diagnosed with a suspected brain tumor. To diagnose and treat the tumor, he was hospitalized at Tokyo Metropolitan Komagome Hospital. Magnetic resonance imaging (MRI) showed a right temporal lobe lesion (see
Magnetic resonance imaging (MRI) scans before and after surgery.
Neuropsychological profile of the patient.
35 | 36 | /36 | |
30 | 27 | /30 | |
Naming | 20 | 20 | /20 |
Repetition | 5 | 5 | /5 |
Comprehension | 10 | 10 | /10 |
Verbal memory | 106 | 125 | |
Visual memory | 91 | 116 | |
General memory | 105 | 126 | |
Attention and concentration | 133 | 127 | |
Delayed recall | 59 | 112 | |
Copy | 36 | 36 | /36 |
Immediate recall | 32 | 31 | /36 |
Forward | 7 | 6 | |
Backward | 7 | 5 | |
12 | 13 | /14 |
The patient completed a recognition test of emotional facial expressions before and after surgery to examine his abilities in this regard. The pre-operative session was performed 3 days prior to the surgery and the post-operative session was performed 4 days after the surgery; therefore, the period between the pre- and post-operative assessments was 7 days. For reference, control subjects were also administered the facial recognition test. The control subjects were recruited from graduate and undergraduate courses and consisted of 23 healthy male volunteers (mean age: 28.6 ± 2.10 years) with no history of neurological disorder. Before the examination, all of the control subjects were informed of the aims of the test, and the authors obtained their written informed consent. The tests were administered at two timepoints with an interval of 1 week, which corresponded with the patient’s interval between tests. The facial expression stimuli included six emotion groups and a neutral group, yielding a total of 54 pictures. The presented emotions and the corresponding numbers of pictures for each emotion were digitalized from the pictures used by
Modified
This study was approved by the Ethics Committee of Tokyo Metropolitan Komagome Hospital (reference number: 1736).
Following surgery, the patient did not display any obvious impairments in standard cognitive abilities, including memory and verbal functions (see
The pre- and post-operative z-scores. The partial credit score for each facial expression was converted into a z-score for each time period based on normative data obtained from 21 normal control subjects.
Percentage score matrix of the expected and observed responses to facial expressions in the control subjects.
Expected to | Surprise | 91.7 | 2.4 | 0.0 | 0.0 | 1.2 | 0.6 | 4.2 |
92.9 | 1.8 | 0.0 | 0.6 | 0.6 | 0.0 | 4.2 | ||
Fear | 55.4 | 25.6 | 4.8 | 8.3 | 0.0 | 5.4 | 0.6 | |
51.8 | 27.4 | 7.7 | 9.5 | 0.0 | 3.6 | 0.0 | ||
Disgust | 0.6 | 0.6 | 45.2 | 37.5 | 1.8 | 0.6 | 13.7 | |
0.0 | 3.0 | 36.9 | 42.3 | 1.2 | 0.0 | 16.7 | ||
Anger | 4.2 | 2.4 | 13.7 | 76.2 | 0.0 | 0.0 | 3.6 | |
3.0 | 1.2 | 14.3 | 75.0 | 0.0 | 0.0 | 6.5 | ||
Happiness | 20.0 | 0.5 | 3.3 | 1.4 | 67.1 | 0.0 | 7.6 | |
18.6 | 1.4 | 3.3 | 0.0 | 68.6 | 0.0 | 8.1 | ||
Sadness | 0.5 | 4.2 | 17.5 | 1.1 | 0.0 | 71.4 | 5.3 | |
0.5 | 5.3 | 18.0 | 1.6 | 0.5 | 69.3 | 4.8 | ||
Neutrality | 3.2 | 1.6 | 4.8 | 15.9 | 0.0 | 0.0 | 74.6 | |
1.6 | 0.0 | 7.9 | 9.5 | 1.6 | 0.0 | 79.4 |
Percentage score matrix of the expected and observed responses to facial expressions in the patient.
Expected to | Surprise | 75.0 | 12.5 | 0.0 | 0.0 | 0.0 | 0.0 | 12.5 |
100.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | ||
Fear | 50.0 | 37.5 | 0.0 | 0.0 | 0.0 | 12.5 | 0.0 | |
87.5 | 12.5 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | ||
Disgust | 0.0 | 0.0 | 50.0 | 37.5 | 0.0 | 0.0 | 12.5 | |
0.0 | 0.0 | 50.0 | 37.5 | 0.0 | 0.0 | 12.5 | ||
Anger | 12.5 | 0.0 | 12.5 | 75.0 | 0.0 | 0.0 | 0.0 | |
0.0 | 0.0 | 0.0 | 100.0 | 0.0 | 0.0 | 0.0 | ||
Happiness | 10.0 | 0.0 | 0.0 | 0.0 | 70.0 | 0.0 | 20.0 | |
20.0 | 0.0 | 10.0 | 0.0 | 70.0 | 0.0 | 0.0 | ||
Sadness | 0.0 | 0.0 | 33.3 | 0.0 | 0.0 | 55.6 | 11.1 | |
0.0 | 0.0 | 11.1 | 0.0 | 0.0 | 88.9 | 0.0 | ||
Neutrality | 0.0 | 0.0 | 0.0 | 33.3 | 0.0 | 0.0 | 66.7 | |
0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 100.0 |
Subtraction score and modified
Furthermore, to evaluate the accuracy of the patient’s performances between pre- and post-surgery, a z-score of the partial credit score was calculated based on the average of two time points in control subjects (see
z-scores of the partial credit scores before and after surgery. The large title refers to the original name of the stimuli and the small title of each of the seven squares represents the responses of patients and controls. The score was converted into a z-score based on 21 normal control subjects. Before surgery, the patient showed a fear bias for surprise stimuli whereas after surgery he showed a surprise bias for fear stimuli. The other six facial expressions remained unchanged compared to before surgery.
We examined the role of the right temporal lobe in the recognition of facial expressions before and after an awake craniotomy. Following the surgery, it was confirmed that the extent of the operation affected the amygdala of the patient and that he showed biased recognition of surprised facial expressions. Compared to previous research, this study has a number of advantages. First, because the patient’s preoperative status was known, we were able to compare the recognition ability before and after surgery. Second, the surgical procedure used was awake craniotomy. Compared to surgery under general anesthesia, awake craniotomy for brain tumors improves safety in terms of preserving neurological function (
It is easy to confuse a surprised facial expression with a fearful one and this phenomenon is related to activity in the right amygdala region (
The present findings are similar to those of
The right amygdala, right posterior central gyrus, and left insula are crucial for the recognition of surprised facial expressions (
Alternatively, several other factors may explain the changes observed in the present study. At his preoperative assessment, the patient exhibited deterioration in the ability to recognize facial expression of surprise. Imaging studies of the amygdala region have revealed activation during the identification of not only fearful facial expressions but also surprised facial expressions (
There are several limitations to the present study that must be noted. First, the present patient was diagnosed with a brain tumor in the temporal region that may have influenced his cognitive abilities. Prior to surgery, the patient exhibited poor recognition of surprised facial expressions as well as poor performance on a delayed recall task. The right amygdala region is related to the recognition of surprised faces (
In conclusion, the present study identified discrepancies in the ability of the patient to recognize facial expressions before versus after the awake craniotomy. Compared to before the surgery, the patient exhibited changes in the ability to recognize surprise. It is our opinion that these results were not due to changes in independent regional function but to disturbances in functional connectivity between the damaged right temporal lobe and the preserved left temporal lobe and among other regions.
The datasets generated for this study are available on request to the corresponding author.
This study was approved by the Ethics Committee of Tokyo Metropolitan Komagome Hospital (reference number: 1736).
AM designed the study, conducted the research, analyzed the data, and wrote the manuscript. SS and CI contributed to the research in their clinical capacity and helped with manuscript preparation. KH contributed to the research on normal subjects. RO contributed to the data analyses and manuscript preparation. RY and NS contributed to the manuscript preparation.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The Supplementary Material for this article can be found online at: