Abstract

Previous work has shown that caloric vestibular stimulation may evoke elementary visual hallucinations in healthy humans, such as different colored lines or dots. Surprisingly, the present case report reveals that the same stimulation can evoke visual hallucinations in a patient with cortical blindness, but with fundamentally different characteristics. The visual hallucinations evoked were complex and came from daily life experiences. Moreover, they did not include other senses beyond vision. This case report suggests that in conditions of cerebral pathology, vestibular–visual interaction may stimulate hallucinogenic subcortical, or undamaged cortical structures, and arouse mechanisms that can generate visual images exclusively.

Introduction

A previous study reported that caloric vestibular stimulation can evoke visual hallucination in healthy humans (Kolev, 1995). The visual hallucinations were of an elementary type—different contours and colors, two-dimensional, or lines and dots, which were stationary in space, but the color, form, and number may change over time.

The current case report was initiated to investigate whether visual phenomenon could be evoked in a patient with cortical blindness. Characteristics of cortical blindness include: (i) loss of visual sensations, (ii) loss of menace reflex (i.e., involuntary blinking that occurs in response to the rapid approach of an object), (iii) preservation of light and accommodation pupillary reflexes, (iv) a normal fundus (i.e., includes the retina, optic disc, and macula), and (v) preservation of ocular movement (Celesia & Brigell, 2005). Ischemic stroke involving the posterior cerebral arteries bilaterally is the most common cause of cortical blindness (Aldrich, Alessi, Beck, & Gilman, 1987).

Subject and Methods

Subject

A 65-year-old male with total cortical blindness caused by a cerebrovascular accident (ischemic necrosis) was studied. On arrival in the emergency department, the patient was conscious. The most prominent damage noted on brain MRI was extensive necrosis in the occipital lobes bilaterally affecting the primary visual cortices. There were smaller areas of infarction in the right thalamus and right internal capsule, periventricular FLAIR hyperintensities around the frontal horns of the lateral ventricles, and bilateral temporal lobe atrophy (see Fig. 1).

Fig. 1.

MRI FLAIR images of the brain. They show: left acute occipital posterior cerebral artery (PCA) ischaemic lesion, right occipital PCA ischaemic lesion, right thalamic and internal capsule ischemic lesions, bilateral temporal atrophy, and periventricular hyperintensities—caps around frontal horns of lateral ventricles.

Fig. 1.

MRI FLAIR images of the brain. They show: left acute occipital posterior cerebral artery (PCA) ischaemic lesion, right occipital PCA ischaemic lesion, right thalamic and internal capsule ischemic lesions, bilateral temporal atrophy, and periventricular hyperintensities—caps around frontal horns of lateral ventricles.

The patient reported that he had totally lost his vision. There was no evidence upon examination, and the patient had no complaints, suggesting that he experienced any symptoms of blindsight. Similarly, there was no evidence of Anton's syndrome (anosognosia for cortical blindness). Pupillary reflexes were intact, suggesting normal functioning of the anterior visual pathways (i.e., optic tracts → pretectal area → Edinger-Westphal nuclei → preganglionic parasympathetic fibers → ciliary ganglia → postganglionic parasympathetic fibers → the pupillary constrictor muscles). Corneal reflexes were also intact. There was no blink response to glabellar tap. Fundoscopic examination was normal. Upon arrival to the emergency department, the patient's blood pressure was 174/92 mmHg. The patient had no spontaneous nystagmus.

The patient reported that he had suffered an initial stroke 7 years ago that manifested with left hemiparesis, from which he had significantly recovered. The patient's other medical history included hyperlipidemia (treated with diet only, no medication), paroxysmal atrial fibrillation (treated with amiodarone), and arterial hypertension (treated with nifedipine) for the past 16 years. There was no other neurological deficit. There was no prior history of any form of psychiatric illness, and the patient had never before experienced hallucinations in any sensory modality. Furthermore, the patient did not experience any hallucinations outside of the vestibular stimulation sessions described below. At the time of the vestibular stimulation procedure, the patient was being treated with an ACE inhibitor, amiodarone, acetylsalicylic acid, and saline solution. None of these medicines have hallucinogenic effects.

Method

Vestibular stimulation was conducted 5 days after an ischemic thromboembolic brain infarction. It was initiated to assess whether the vestibulo-ocular reflex (VOR) was present, to check for any pathologic VOR asymmetry, and to determine if there were any visual–perceptual changes. The study was conducted in a dark room. The applied vestibular stimulus consisted of 20°C (68°F) water irrigation; 150 cc for 30 s in each ear in alternation in supine position with the head raised at 30° above the horizon. Both labyrinths reacted to the calorics, and there was no pathological VOR asymmetry. Informed consent to study the visual-perceptive manifestations of vestibular stimulation was obtained from the patient .The study was approved by the local ethics committee and was performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki.

Results

All calorics provoked strong nystagmus, which were recorded with conventional nystagmography. The patient did not report vertigo or dizziness following calorization.

The calorics evoked visual hallucinations as described in Table 1. The hallucinations began ∼1 min after initiation of the calorization.

Table 1.

Hallucinations of the patient with cortical blindness

Right ear caloric stimulations Left ear caloric stimulations 
1. “I see a brown cat with open eyes, standing quietly on four legs, without meowing … I have never seen this cat before.” (The hallucinatory image lasted for ∼1 min.) 2. “I see a book with cubes … The image has changed to a stationary grid in front of me, in black, white and yellow … The form has changed to a pyramid ….” In the second minute: “I see a kitten which has gone under my belly.” (The image lasted ∼1.5 min.) 
3. “I see letters –, e.g., ‘Д’, ‘Т’ (Cyrillic alphabet)—moving on something like a white screen.” (The image lasted 20 s.) “Now I see brown table with no tablecloth, with chairs around it.” (The image lasted 24 s.) 4. “I see stone masonry and water ….” (The image lasted 16 s.) “Now I see a spoon falling on the network … I see a streaky brown hat—motionless.” (The image lasted ∼1 min.) 
5. “I see different colors … Now I see different animals.” (The image lasted ∼80 s.) 6. “I see light—it is bright … it faded after a while … a cat on a box, a dark box. The cat is on the left. It sits there, not moving, alive, opening its mouth without moving its head. Now I see crate with vegetables—onions, cucumbers.” (The image lasted ∼1.5 min.) 
7. “In front of my eyes it's becoming brighter; To the right I see the iron frame of a bed … a brown box with clear water.” On the 126th second: “I see bag of seeds in the box.” (The last image lasted ∼50 s.) 8. “I see in front of my eyes colors like rainbow… brown and green spots.” On 120th second: “Now a cat has appeared, standing on the table, making no sounds … Now it is walking.” (The last image lasted ∼1.5 min.) 
Right ear caloric stimulations Left ear caloric stimulations 
1. “I see a brown cat with open eyes, standing quietly on four legs, without meowing … I have never seen this cat before.” (The hallucinatory image lasted for ∼1 min.) 2. “I see a book with cubes … The image has changed to a stationary grid in front of me, in black, white and yellow … The form has changed to a pyramid ….” In the second minute: “I see a kitten which has gone under my belly.” (The image lasted ∼1.5 min.) 
3. “I see letters –, e.g., ‘Д’, ‘Т’ (Cyrillic alphabet)—moving on something like a white screen.” (The image lasted 20 s.) “Now I see brown table with no tablecloth, with chairs around it.” (The image lasted 24 s.) 4. “I see stone masonry and water ….” (The image lasted 16 s.) “Now I see a spoon falling on the network … I see a streaky brown hat—motionless.” (The image lasted ∼1 min.) 
5. “I see different colors … Now I see different animals.” (The image lasted ∼80 s.) 6. “I see light—it is bright … it faded after a while … a cat on a box, a dark box. The cat is on the left. It sits there, not moving, alive, opening its mouth without moving its head. Now I see crate with vegetables—onions, cucumbers.” (The image lasted ∼1.5 min.) 
7. “In front of my eyes it's becoming brighter; To the right I see the iron frame of a bed … a brown box with clear water.” On the 126th second: “I see bag of seeds in the box.” (The last image lasted ∼50 s.) 8. “I see in front of my eyes colors like rainbow… brown and green spots.” On 120th second: “Now a cat has appeared, standing on the table, making no sounds … Now it is walking.” (The last image lasted ∼1.5 min.) 

Unlike the vestibularly evoked visual hallucinations in healthy humans, the hallucinations in this patient with cortical blindness were complex. The hallucinations were three-dimensional, colored, lasted several seconds up to 1 min, and then immediately changed into other images, which were unrelated to the previous hallucinations. They were visual images derived from the environment of daily life.

There was no motion related to the direction of the evoked nystagmus. Patient report revealed the images contained animals or inanimate objects. There were no images of humans. Only the images of animals moved, but even when not moving, the animals looked alive. Some of the hallucinatory images reappear in repeated calorics but were not specific to the irrigated ear, nor necessarily to the immediate consequent irrigation. The hallucinatory images were either stationary or moving in space. Interestingly, there were no associated sounds with the hallucinations; the patient reported that it was like watching silent movies. No smells were reported either.

Discussion

This case study raises questions about where and how the vestibularly evoked visual hallucinations seen in this case are generated in patients with cortical blindness. The following hypotheses are suggested to explain the genesis of these hallucinations. The vestibular stimulation evoked afferent excitatory impulses to the subcortical visual regions of the brain and to the residual undamaged, or partially damaged, visual cortical structures. In healthy subjects, the visual cortex probably suppresses irritative vestibular impulses. Brandt, Bartenstein, Janek, and Dieterich (1998) hypothesized that in healthy humans there is reciprocal inhibitory visual–vestibular interaction, and Ajina, Kennard, Rees, and Bridge (2015) noted that top-down signals from higher visual areas could cause suppression of vestibular impulses. When the visual cortex is damaged, the normal inhibition or suppression does not function properly. This allows strong vestibular impulses to cause abnormal excitation in the residual undamaged, and partially damaged, cortical and subcortical structures.

The discussion that follows will briefly mention some of the possible structures and pathways that could trigger the described hallucinatory phenomena. Beginning with the phylogenetically older extrageniculate pathways, the superior colliculi are considered to perform an integrative function, and according to some investigators (Merker, 2007; Sewards & Sewards, 2000), contain a primary visual representation of the world. Higher integrative centers in the diencephalon and telencephalon may also play a role (Bottini et al., 2001; Dieterich, Bucher, Seelos, & Brandt, 1998; Lopez & Blanke, 2011). Emerging from the superior colliculi are pathways that project to the pulvinar nucleus of the thalamus, and relevant to this discussion, vestibular sensitive neurons have been found in the anterior and lateral pulvinar (Lopez & Blanke, 2011). The pulvinar is a ‘relay’ processing center that projects to posterior cortical regions and passes information from one cortical area to another, thereby modulating cortical activity. Furthermore, the medial pulvinar has been found to be activated during caloric vestibular stimulation (Bottini et al., 2001). Pulvinar activation has also been reported during optokinetic stimulation (Dieterich et al., 1998), suggesting the importance of this thalamic nucleus for multisensory integration of vestibular and visual signals.

Vestibular projections also terminate in the lateral geniculate nucleus of the thalamus, which in turn has reciprocal connections with the visual cortices (areas 17, 18, and 19) and is also considered as a ‘relay’ passing visual information to the cerebral cortex (Lopez & Blanke, 2011). In addition, there are vestibular pathways that terminate in the lateral dorsal nucleus of the thalamus, which also project to the visual cortices. Thus, the thalamus is integrally involved in vestibulo–visual interaction signal processing within cortico-thalamo-cortical loops (Lopez & Blanke, 2011).

With respect to the connections of subcortical areas with secondary visual association (extrastriate) cortices, numerous primate studies have suggested that direct visual routes may exist from both the lateral geniculate nucleus and superior colliculus/pulvinar to extrastriate cortex (V3, V4, V5/MT+ for example), and some of these connections are thought to underlie the blindsight phenomenon (Cowey, 2010). It is likely that under normal circumstances, these subcortical to visual association area connections are overshadowed by overwhelming input from the primary visual cortices in V1 (Ajina et al., 2015; Schmid et al., 2010). It is possible the blindsight and the vestibularly evoked visual hallucinations use similar, or perhaps identical, pathways but the vestibular input evoking hallucinations is probably a stronger stimulus with different characteristics.

When there is damage to the visual cortices, decentralization of visual functions may occur. Vestibular impulses could then possibly evoke hallucinatory visual images that have been stored in the visual regions of the brain. Alternatively, it is possible that the residual visual structures may function paradoxically (in a phasic state), and create a situation where routine vestibular stimulation may cause a paradoxically stronger response that could generate visual hallucinations. This abnormal excitation would presumably reverberate for a period of time because the hallucinations in the present case lasted up to 1 min.

It is important to stress that the patient did not experience self-motion illusions, or hallucinatory images of motion, although vestibular stimulation produced robust nystagmus. This indicates that when the visual cortex is damaged, the vestibular–visual interaction for perception of motion in space does not function properly to create generally existing vestibularly evoked vection (i.e., a sense of motion fused into an image) (Kolev, 2001–2002). Finally in addition to these extrageniculate subcortical structures and pathways, other mechanisms should also be taken into account such as the possibility that vestibular irritations could cause microcirculatory and metabolic changes in the visual structures of the brain (Tiecks, Planck, Haberl, & Brandt, 1996), which in turn might facilitate the generation of hallucinations.

Conclusion

This case report revealed a relatively unknown brain mechanism of vestibulo-visual interaction at a perceptual level that involve the extrageniculate subcortical visual structures and possibly the residual damaged portions of the primary visual cortices. In the context of cortical blindness, these alternative pathways and subcortical structures may stimulate hallucinogenic structures that generate visual images exclusively; that is, without the involvement of other senses.

Acknowledgements

The author thanks to Dr L. Haralanov who first examined and diagnosed the patient and to Dr N. Topalov for MRI images and report. The author gratefully acknowledges the constructive comments and suggestions of the editors and reviewers for this article, which significantly improved the manuscript.

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