Phantom percepts: tinnitus and pain as persisting aversive memory networks

Abstract

Phantom perception refers to the conscious awareness of a percept in the absence of an external stimulus. On the basis of basic neuroscience on perception and clinical research in phantom pain and phantom sound, we propose a working model for their origin. Sensory deafferentation results in high-frequency, gamma band, synchronized neuronal activity in the sensory cortex. This activity becomes a conscious percept only if it is connected to larger coactivated "(self-)awareness" and "salience" brain networks. Through the involvement of learning mechanisms, the phantom percept becomes associated to distress, which in turn is reflected by a simultaneously coactivated nonspecific distress network consisting of the anterior cingulate cortex, anterior insula, and amygdala. Memory mechanisms play a role in the persistence of the awareness of the phantom percept, as well as in the reinforcement of the associated distress. Thus, different dynamic overlapping brain networks should be considered as targets for the treatment of this disorder.

Fig. 1.

Brain networks involved in phantom perception. Sensory deafferentation causes neuroplastic changes resulting in increased activation of the primary sensory cortex: somatosensory cortex (gray) in the case of phantom pain and auditory cortex (brown) in the case of tinnitus. Awareness of the stimulus arises when this activity is connected to a larger coactivated awareness or perceptual network. This perceptual network involves subgenual (sgACC) and dorsal anterior cingulate cortex (dACC) and posterior cingulate cortex (PCC), precuneus, parietal cortex, and frontal cortex (blue). Salience to the phantom percept is reflected by activation of dACC and anterior insula (yellow). As a consequence of a constant learning process, the phantom percept becomes associated to distress, which is reflected by a nonspecific distress network consisting of the anterior cingulate cortex (sgACC and dACC), anterior insula, and amygdala (red). The persistence of the phantom percept is due to memory mechanisms involving the parahippocampal area, amygdala, and hippocampus (green).