Disorders of Sensory Input Associated with Hallucinations

Hallucinations produced by disorders of the peripheral sensory system appear to result from ongoing cortical sensory processing in the setting of degraded or absent sensory input. Sometimes referred to as "release" phenomena, the use of the term in this context can be misleading because it has traditionally been used to connote neural activity released by the failure of higher level inhibitory centers rather than by disordered lower level input. The probable mechanism by which these hallucinations are generated is best understood by considering the interplay between peripheral and central processing in normal perception. Although the previous description of sensory processing emphasizes the flow of information from periphery to thalamus to cortex ("bottom-up" processing), the connections between thalamus and cortex are in fact bidirectional, as noted. This pattern of connectivity enables the cortex to play a role in selecting from among the massive array of inputs to the thalamus those most likely to be relevant in light of past and current experience. Thus, perceptions arise from an interplay between cortically generated expectations ("top-down" processing) and data (confirmatory or otherwise) from peripheral sensory receptors. In this setting, a dearth of peripheral input might give rise to perceptions dominated by expectations rather than current environmental conditions.

Hallucinations caused by disordered peripheral input are most frequently seen in the visual system. The term Charles Bonnet syndrome has been applied to such phenomena, but without a consistent definition. The hallucinations are most often vivid, colorful, and complex representations of people, animals, scenery, trees, buildings, or flowers that fill the entire visual field. They frequently appear smaller than normal, or Lilliputian, and may move. Hallucinations tend to have an abrupt onset, can last seconds to hours, and may disappear with movement or closure of the eyes. They can occur in the setting of acute blindness following altered blood flow or trauma to the eye, a phenomenon sometimes referred to as phantom vision, or during a gradual visual decline. In either case, they may fade as the visual disturbance continues. Notably, the individuals experiencing the hallucinations are aware that they do not represent reality and generally have no strong emotional association or reaction to them. Although primary abnormalities within the central nervous system may increase the risk of developing Charles Bonnet syndrome (a hypothesis supported by its greater prevalence in the elderly, who are at increased risk of subtle brain dysfunction), it can occur on the sole basis of peripheral visual system dysfunction. Indeed, its prevalence rate of 20% in people who develop blindness is similar to the 19% of normal individuals who experience visual hallucinations during sensory deprivation experiments—a clear example of hallucinations caused solely by disordered peripheral input.

Conditions such as stroke, that involve destruction of primary visual cortex or the cerebral pathways leading to it can also lead to complex visual hallucinations. Although the lesion in this instance is central, the phenomenology and mechanism are similar to those seen with peripheral lesions because primary visual cortex provides input to the unimodal association areas involved in the generation of complex hallucinations. The major phenomenologic difference derives from the organization of visual processing in primary cortex, where the right visual field is mediated by left occipital cortex and vice versa. When central lesions are limited to one hemisphere, hallucinations occur only in the affected contralateral visual field.

In the somatosensory system, a striking example of hallucinations caused by disordered sensory input occurs in the phantom limb syndrome, as described by Melzack. After amputation of a limb, approximately 95% of adults experience the limb as still present, able to move in space, and to feel pain or tingling. Over time, the perception weakens such that the proximal part of the limb no longer seems to exist, leaving the hand or foot hanging in midair, or the entire limb seems to "telescope" into the body, leaving the hand or foot directly connected to the stump. Phantom experiences have also been reported after the loss of eyes, teeth, external genitalia, and breasts. They are not dependent on sensory input from the residual scar and can occur even in those with congenitally absent limbs, suggesting a central representation of the body that is at least partly innate.

In the auditory system, individuals with peripheral dysfunction can develop complex hallucinations, such as music (either instrumental or vocal) or voices, or simple hallucinations, such as ringing, buzzing, or isolated tones of various pitches. Although more common with bilateral dysfunction, hallucinations can accompany unilateral peripheral auditory disease, in which case they are experienced as emanating from the affected side.

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