Medial limbic brain damage selectively impairs affect decoding from normal and whispered voices

The medial temporal lobe (MTL) is crucial for recognizing emotions from various communicative signals, such as voice intonations. It is also a common source of intractable epileptic seizures, and patients undergoing MTL resection are potentially affected by a variety of cognitive and affective deficits depending on the location and size of MTL lesions. This study aimed to identify specific subregions within the MTL where associated lesions lead to deficits in emotional recognition from vocal utterances. This study had a specific emphasis on comparing emotional recognition from normal and from degraded voice signaling, such as in vocal whispering. The latter was assumed to rely on a more extensive processing in MTL regions given the impoverished acoustic signal in whispers. Twenty patients, who underwent unilateral MTL resection targeting the amygdala and hippocampus, and twenty matched healthy controls, were compared using an auditory emotion recognition task from vocal utterances. Participants were asked to recognize and classify the angry, fearful, or neutral tone from whispered or normal vocal utterances. MTL lesion location and spatial extent in patients were determined based on anatomical brain scans, and voxel-based lesion-symptom mapping (VLSM) analysis was applied. The key findings were that patients generally performed similarly to the control group in the emotion recognition task, except in the fear recognition condition. The brain-behavior analysis revealed that an MTL subregion at the junction between the amygdala and hippocampus was associated with deficits in recognizing emotions from whispered voices. Overall, circumscribed MTL lesions can impair emotion recognition from whispered vocalizations to some degree, pointing to the relevance of an integrated amygdala-hippocampal complex for the accurate recognition of emotions from various vocalization types.