A Five-Year-Old Child With Bilateral Amygdala Loss

The patient, a 5-year-old, ethnically Chinese boy, presented with a history of aggressive behavior. He was referred by his neurologist where the diagnosis of ESES (electrical status epilepticus of sleep)¹³ was made, and a neurodegenerative process was identified with unknown etiology.

Our patient was found on the streets of Beijing at the estimated age of 2 weeks, after apparently being abandoned by his biological parents. He was cared for in an orphanage for 18 months and was subsequently adopted by an American couple. He presented with some dysmorphic features (a malformed ear and a slightly asymmetrical face), and a weak right arm due to mild cerebral palsy. After being with his adoptive parents for about 5 months, our patient began to refuse to be fed and seemed to have lost all interest in food. Because of concerns about failure to thrive, this ultimately led to the placement of a gastric feeding tube. Aggressive behaviors were another clinical concern and were initially assumed to be related to disordered attachment related to early experience in an orphanage setting. Although there was no clear loss of acquired language or other skills, parental concerns about delayed development resulted in a neurological evaluation, including an MRI, which revealed some atrophy of medial temporal structures initially. A follow-up MRI 2 years later showed progressive, extensive loss of these same structures (Figure 1).

At the time of the initial interview, the parents reported that our patient had a history of spontaneous, apparently unprovoked aggression associated with inappropriate affect (for example, smiling while pulling out clumps of his sibling’s hair). They also reported no interest in food, no significant mood disturbances, and little-or-no fear. The parents reported both a lack of fear toward strangers and a lack of fear in association with environmental dangers such as falling from heights. According to the parents, he could communicate his needs, but could not speak using words. They reported minimal interaction with other children, very limited shared play, and very simple, mostly a mechanistic, perseverative play, characterized by manipulation of his toys for minutes or even hours. Although his social interactions were not as complex as those of his peers, he would make eye contact readily and seemed to enjoy the company of his family, as evidenced by proximity-seeking and affective reciprocity.

Screening evaluations of autistic behaviors were performed with the M-CHAT and Social Reciprocity Scale (SRS). On the M-CHAT, the patient failed 4 items, and on the SRS completed by the parents, the patient scored well within the clinical range (101 and 104, respectively).

Observation of the patient with his primary caregivers revealed a wide variety of social behaviors. When observed with his mother alone, the patient displayed good eye contact and sharing of play activities. However, when an unknown female examiner entered the room and his mother left the room, the patient immediately dove underneath a table. After few minutes, the boy did begin to interact with the female examiner, rolling a ball back and forth with her and laughing. When the mother returned, the boy was clearly glad to see her, again making good eye contact and smiling.

This 5-year-old boy presented with a combination of complex behavioral problems, including developmental delays, markedly impaired expressive language and limited receptive language abilities, refusal to eat, seizures, limited social reciprocity with a history of ritualized social interaction, and aggression. His aggression improved with treatment of his seizures, but was still present—although at a markedly reduced level—at the time of evaluation. His aggressive behavior and his refusal to eat were interesting, given his bilateral amygdala damage, as this kind of lesion has been typically reported to be associated with apathy and hyperphagia in the Kluver-Bucy syndrome.¹⁴

Despite the absence of amygdala bilaterally, our patient did evidence anxiety in social settings and did engage in some complex reciprocal social interactions, although it is clear that these interactions were not as well developed and complex as those known in age-matched peers. Despite his adoptive parents’ recounting of overall fearlessness and a lack of stranger anxiety, he did show anxiety when in the presence of strangers, and exhibited this anxiety, for example, by withdrawing completely from the situation, as he did when he hid underneath the table when confronted by a strange examiner.

The presence of social anxiety as well as social competence in our patient argues against the notion that an intact amygdala is required for these complex behaviors. Our patient did clearly exhibit some impaired social interactions, but he was able to interact meaningfully with his caretakers, show preference for primary caregivers, and even show shared, friendly play with a stranger. The conservation of complex emotional behaviors despite the nearly complete loss of the amygdala bilaterally argues for the plasticity and redundancy of the cortical substrates that serve emotional processing in the human brain. This case shows the importance of early childhood competency in emotional processing by showing how robust the systems serving this ability must be, allowing remarkable adaptation even in the face of radical structural abnormalities in the brain. Findings suggest that compensatory mechanisms are possible in the brain emotion system early in life.