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Behavioral Disconnection Syndrome Manifesting as Combined Mania and Visual-Auditory Hallucinations Secondary to Isolated Right Thalamic Hemorrhage

2017; American Psychiatric Association Publishing; Volume: 29; Issue: 4 Linguagem: Inglês

10.1176/appi.neuropsych.16110308

1545-7222

Parunyou Julayanont, Doungporn Ruthirago, Khondoker Alam, Yazan J. Alderazi,

Advanced Neuroimaging Techniques and Applications

Back to table of contents Previous article Next article Case ReportsFull AccessBehavioral Disconnection Syndrome Manifesting as Combined Mania and Visual-Auditory Hallucinations Secondary to Isolated Right Thalamic HemorrhageParunyou Julayanont, M.D., Doungporn Ruthirago, M.D., Khondoker Alam, M.D., Yazan J. Alderazi, M.D.Parunyou Julayanont, M.D., Doungporn Ruthirago, M.D., Khondoker Alam, M.D., Yazan J. Alderazi, M.D.Published Online:15 Mar 2017https://doi.org/10.1176/appi.neuropsych.16110308AboutSectionsPDF/EPUB ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InEmail Damage to the thalamus can contribute to the phenomenon of diaschisis manifesting as various behavioral symptoms. We present the case of a 55-year-old man who presented with acute mania and late-onset combined visual and auditory hallucinations after right thalamic hemorrhage. This is the first report, to our knowledge, of a combination of mania and visual-auditory hallucination in a patient with isolated thalamic damage. Details of all previous case reports on isolated thalamic damage presenting with mania or hallucination are provided. We propose the networks of diencephalic damage causing mania and hallucinations, which represent the behavioral disconnection syndromes.It is challenging to localize a single lesion when neuropsychiatric symptoms are the only manifestations. The thalamus is a complex structure connecting between the brainstem and various cortical areas. Damage to the thalamus can contribute to various behavioral conditions. We report the first case, to our knowledge, of a patient who suffered from right thalamic hemorrhage presenting with combined acute mania and visual-auditory hallucinations. The case broadens the clinical approach on the behavioral disturbance secondary to focal brain lesion on the thalamus. We also systematically review the previous reports on the cases of isolated thalamic damage with mania or hallucination. Finally, we provide the proposed networks of diencephalic damage causing mania and hallucinations.Case ReportA 55-year-old man without a previous history of psychiatric conditions or substance abuse presented with a 1-week history of acute mania. He had irritability, grandiosity, combative speech, paranoid delusion, high energy levels, decreased need for sleep, pressurized speech, euphoria, and inappropriate cheerfulness. The patient had been a mild-mannered and composed person prior to this event. Neurological examination showed no focal neurologic deficits; urine drug screen was negative; MRI showed cavernous malformation with hemorrhage involving the dorsomedial and pulvinar nucleus of the right thalamus (Figure 1); and electroencephalography was normal. Risperidone was started. At 4 months follow-up, the manic symptoms resolved, and risperidone was discontinued.FIGURE 1. MRI Head Showing the Cavernous Malformation Hemorrhage on the Right Thalamus Involving the Dorsomedial and Pulvinar Nucleiaa The image shows A) axial view on the fluid-attenuated inversion recovery sequence; B) axial view on the gradient-echo sequence; and C) sagittal view on the T1 sequence.One year later, he presented with acute psychosis. He had vividly visual hallucination (transient texts on his phone, unknown people and colorful airplanes). He also reported the musical hallucination that he heard pleasant classical music in particular at night. He denied any commanding or voice hallucination. He had hypnagogic visual and musical hallucinations. He has insight to the hallucinations. MRI head demonstrated stable cavernous malformation (Figure 1). Risperidone was resumed and effectively improved hallucination within a week.DiscussionManiaMania after thalamic lesions has been described in a small number of patients. Symptoms of mania secondary to focal brain lesions are clinically similar to the features of primary psychiatric mania. Some features may help localizing lesions to the thalamus or differentiating from primary mania, such as hemianesthesia, hemiparesis, hypersomnolence, abnormal movement, abnormal gaze, and amnesia.From literature review, we found 18 cases of mania (including our case) caused by isolated thalamic lesions on various thalamic nuclei, including the dorsomedial, intralaminar, pulvinar, anterior, ventrolateral, and ventromedial nuclei (Table 1). It is interesting that, in all of these cases, the lesions involved the right thalamus, with the isolated right thalamus in 72% (N=13/18) of cases and both thalami in 28% (N=5/18) of cases. The majority of patients (80%) developed mania immediately or within a few days after the damage; however, late-onset mania may occur up to many months after the events. In cases with mild symptoms, patients usually spontaneously recover without medication. In more severe cases, mood stabilizers or atypical antipsychotics are effective treatment. Even though most of the reported patients did not have recurrent mania, a minority of the cases developed hypomania or cyclic depression-mania during the follow-up period.TABLE 1. Cases With Isolated Thalamic Damage Causing ManiaStudySexAge (Years)LocationsHemisphereOnsetEtiologiesManic SymptomsAssociated SymptomsTreatmentCummings et al.13Two casesNAUnspecifiedRightAcuteIschemic strokeCase 1: euphoria, talkativeness, hypersexuality, euphoric, irritable, and poor judgementHemisensory loss, amnesia, denial of illness, and depression (case 2)Lithium in one case with improvement; no medication in one caseCase 2: euphoric, decreased need for sleep, and preoccupied with religionGentilini et al.14Male66ParamedianRight and LeftAcuteIschemic StrokeHypersexuality, grandiosity, and cheerfulnessAmnesia, somnolence, and delusionNot reportedFemale47ParamedianRight and LeftAcuteIschemic strokeHyperphagia, euphoria, and childish behaviorsHypersomnolence, abnormal eye movement, and depressionNot reportedMale35ParamedianRight and LeftAcuteIschemic strokeHyperphagia and irritabilityAmnesiaNot reportedBogousslavsky et al.6Female72Paramedian, dorsomedial and ventral lateralRightAcuteIschemic strokeSmiling and inappropriate laughing and jokes, logorrhea, rapid switching of ideas, lack of spontaneity, and disinhibitionHypersomnolence, disorientation,Not reportedStarkstein et al.15Three casesNAUnspecifiedRightNAHemorrhage and ischemic strokeMania (unspecified symptoms in each case)NANAKulisevsky et al.16Female81Ventral lateral and ventromedialRightAcuteIschemic strokeEuphoria, talkativeness, grandiosity, flight of ideas, inappropriate jokes, and decreased need for sleepLeft hemichoreaHaloperidol with improvement after 4 weeksMcGilchrist et al.17Male43ParamedianRight and LeftAcuteIschemic strokeCyclic elation, hypersexuality, hyperphagia, flight of ideas, and decreased need for sleepHypersomnolence, cyclical apathy and depressionNot reportedDaum et al.18NA64AnteriorRightAcuteIschemic StrokeHypersexuality, talkativeness, irritability, mood fluctuation, and verbal aggressionAmnesiaNot reportedVuilleumier et al.19Male63UnspecifiedRightAcuteIschemic strokeMania episode followed by hypomaniaProsopoaffective agnosiaNot reportedLeibson20Male53UnspecifiedRightAcuteHemorrhageTalkativeness, cheerfulness, hypersexuality, and increased energyAnosognosia, headache and left-sided numbness and weakness, gaze problem, and hemineglect,Resolved 10 weeks after the strokeInzelberg et al.21Male61PulvinarRightAcuteIschemic strokeEuphoria, talkativeness, disinhibition, flight of ideas, hypersexuality, decreased need for sleep, and increased goal-directed activityLeft hemichoreaHaloperidol with improvement after 8 weeksBenke et al.7Male38Dorsomedial, intralaminar and anteriorRight and Left4 weeksIschemic strokeLogorrhea, restlessness, mood elevation, inflated self-esteem, reduced need for food and sleep, and hypersexualityAmnesia, vertical gaze paralysis, and dysarthriaLow-dose neuroleptic with improvement after 8 weeksLopez et al8Male63UnspecifiedRight5 monthsIschemic strokeCyclic maniaBipolar symptoms with cyclic depression, and melancholic stuporRisperidone, valproic acid, and quetiapine for maniaRouth and Hill22Male83PosteriorRight2 weeksHemorrhageAggressiveness, speech disinhibition, talkativeness, flight of ideas, and inflated self-esteemParanoid delusionsOlanzapineJulayanont et al. (current case)Male55Dorsomedial and pulvinarRightAcuteHemorrhageIrritability, grandiosity, combative speech, high-energy levels, decreased need for sleep, pressurized speech, euphoria, and inappropriate cheerfulnessParanoid delusions and amnesiaRisperidone with improvement after 4 weeksTABLE 1. Cases With Isolated Thalamic Damage Causing ManiaEnlarge tablePeduncular HallucinosisPeduncular hallucinosis classically presents with vivid visual hallucination usually with preserved insight. Midbrain damage with or without thalamic involvement is the typical origin of hallucination. Isolated thalamic lesions were rarely reported to cause this condition (Table 2). From the literature review, we found 15 cases (including our case) of hallucinations secondary to isolated thalamic damage. Even though there is no specific thalamic nucleus consistently reported to cause peduncular hallucinosis, the dorsomedial (46%, N=6/13 cases), pulvinar (31%, N=4/13 cases), and anterior (15%, N=2/15 cases) nuclei are the common locations contributing to this condition (Table 2). Unlike mania, there is no relationship between the side of diencephalic lesions and hallucinations. From 15 case reports, the lesions were on the right side in 47% (N=7/15 cases), on the left side in 47% (N=7/15 cases), and on both sides in 6% (N=1/15 case). Similar to mania, the majority of peduncular hallucinosis (66%, N=10/15 cases) occurred within the first week after damages, but late-onset can present up to a year as reported in our case. Atypical antipsychotics are the drug of choice in severe cases.TABLE 2. Cases With Isolated Thalamic Damage Causing HallucinationsStudySexAge (Years)LocationsHemisphereEtiologiesOnsetHallucination FeaturesAssociated SymptomsTreatmentVisualAuditoryFeinberg and Rapcsak23Male83DorsomedialRightIschemic strokeAcuteAnimals in his house (flying birds and dogs), military marching, girls in an examination roomNoVertigo, ataxic gaitResolved in 1 weekSerra et al.24Male68PosteriorRightIschemic strokeAcuteAnimals and men's headNoLeft hemiparesis, paraesthesiasNot reportedInzelberg et al.25Female75UnspecifiedLeftIschemic stroke2–3 daysNoMusical hallucination of popular songs from her youthRight hemiparesis and dysphasiaImproved with no reported treatmentNoda et al.26Male72DorsomedialRightIschemic stroke3 daysVivid recollection of his old job, dish of sweet potatoes and cigarette between his fingersNoHypersomnolence and nocturnal insomniaResolved over 2 weeks with no reported treatmentFemale46AnteriorLeftIschemic stroke4 daysParents who passed away 10 years ago, teapot and teacups on a tableCommanding voice: "Don't eat"Memory impairment, right upper limb weaknessResolved over 2 weeks with no reported treatmentManford and Anderson27Male58PulvinarRightIschemic stroke10 daysBall of light, a man in a suit, a black butterfly, dwarves, striped fish swimmingNoNoNot reportedYoshida et al.28Female73DorsomedialLeftIschemic stroke2 monthsNoVoices telling her about misfortunes, voices of threats and commands,Anterograde and retrograde amnesiaRisperidone and olanzapineMollet et al.29Female61LateralRightIschemic strokeAcuteCollege-age boys in colorful Hawaiian shirts, men in black religious clothesConversation between college boysPain and numbness at the left hemibodyNot reportedGüzelcan et al.30Male46UnspecifiedrightTumorNot reportedParades of people, seeing spiders, mice runningNoNoRisperidoneMittal and Khan31Female19VentroanteriorLeftIschemic strokeAcuteNoCommanding VoicesConfusion, flat affect, imaginary boyfriend, and paranoid delusionRisperidoneLee et al.32Male20AnteriorleftIschemic strokeAcuteDangerous hands and snakesNoAmnesia, anomia, and depersonalizationNot reportedFornazzari et al.12Male45Lateral and posteriorLeftHemorrhage9 monthsSound-tactile, sound-color, and grapheme-gustatory synesthesiasNoNot reportedDelgado and Bogousslavsky33Male61DorsomedialLeftIschemic strokeAcuteBody distortion above the waist, lights and mice running down the wallNoTransient perioral and left paresthesiasDisappeared without treatmentFemale48ParamedianRight and Left (right >left)Ischemic strokeAcuteNoVoice and noise distortion made by "dinosaurs"DisorientationDisappeared without treatmentJulayanont et al. (current case)Male55Dorsomedial and pulvinarRightHemorrhage12 monthsTransient texts on his phone, unknown people and colorful airplanesMusical hallucinationParanoid delusions and amnesiaRisperidoneTABLE 2. Cases With Isolated Thalamic Damage Causing HallucinationsEnlarge tableEven though visual hallucination is the classic type of peduncular hallucinosis, auditory hallucinations also occur after diencephalic damage. To our knowledge, there have been only two case reports of combined visual and auditory hallucinations secondary to isolated thalamic lesions, which involved the anterior and lateral nuclei in each case. Our case is the first report of damage to the dorsomedial and pulvinar nuclei contributing to combined hallucinations.Network Model of Mania and Hallucinations Secondary to Thalamic InsultsMania secondary to diencephalic lesions derives from the phenomenon of diaschisis that is caused by disconnection of the thalamus from the thalamo-prefrontal-limbic networks. The magnocellular (medial) part of the dorsomedial nucleus connects the thalamus with the limbic system via the orbitofrontal cortex.1 Damage to this network causes disinhibition of inappropriate behaviors and enhanced reward-seeking behaviors.2 The medial part of the dorsomedial nucleus also projects the neuronal network to the amygdala via the amygdalofugal tract, and thus a lesion on this nucleus can lead to emotional dysregulation, aggression, increased oral intake, and hypersexuality. In addition, damage to the intermediate part of dorsomedial nucleus, which links to the dorsolateral prefrontal cortex, can contribute to executive dysfunction.Damage to the anterior nucleus, which is connected to the mammillary bodies and amygdala via the mamillothalamic and ventral amygdalothalamic tract, respectively, causes problem with emotional expression and dysregulation of motivation.1 The pulvinar nucleus is an associative nucleus connecting to multiple cortical areas.1 The medial part of the pulvinar nucleus sends some connections to the anterior insular cortex and functions in controlling emotional awareness that is required for emotional regulation.3 Some fibers from the intermediate part of the pulvinar nucleus also project to the dorsolateral prefrontal cortex and take part in executive performance.The role of the right thalamus in the pathogenesis of mania is supported by previous studies demonstrating decreased right thalamic volume in patients with bipolar disorder compared with normal controls4,5 and reduced right thalamic and ipsilateral prefrontal/orbitofrontal perfusion in cases with diencephalic mania.6–8 It is hypothesized that emotional regulation is lateralized, with the right hemisphere controlling negative moods and the left hemisphere controlling positive emotions. The interhemispheric imbalance, with left-sided hyperfunction and right-sided hypofunction, on the prefrontal, orbitofrontal, and insular cortices, may contribute to the emotional releasing effect from the contralesional side and result in secondary mania.9,10Similar to mania, the diaschisis of neural networks also explains the pathogenesis of peduncular hallucinosis. In the classic peduncular hallucinosis from mesencephalic lesions, the disruption along the pathway from the ascending reticular activating system in the brainstem to the thalamus may contribute to the hallucinations. While in the cases with thalamic lesions, dysregulation between the thalamus and the extrastriate cortex and superior temporal gyrus leads to visual and auditory hallucination, respectively. This hypothesis is supported by a study on the lesion-based resting-state networks, which showed the maximal network overlap for visual hallucinations on the extrastriate visual cortex and for auditory hallucinations on the superior temporal gyrus.11The pulvinar nucleus is the multimodal integrative nucleus connecting to the posterior parietal, superior temporal, and extrastriate cortices. Damage to this structure may also cause problems with somatosensory-auditory-visual integration, resulting in multimodal hallucinations. The lateral posterior nucleus was reported to cause multimodal somatosensory-visual-auditory-gustatory synesthesia.12We propose the network explaining the pathogenesis of mania and peduncular hallucinosis secondary to thalamic lesions (see Figure 2).FIGURE 2. Proposed Network of Mania and Peduncular Hallucinosis Secondary to Thalamic LesionsFrom the Department of Neurology, Texas Tech University Health Sciences Center, Lubbock, Tex. 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A Case-Related Review of the Literature on Peduncular Hallucinosis Following Intracerebral Hemorrhage12 August 2021 | Clinical and Translational Neuroscience, Vol. 5, No. 2Right-sided brain lesions predominate among patients with lesional mania: evidence from a systematic review and pooled lesion analysis12 May 2020 | Translational Psychiatry, Vol. 10, No. 1Mapping mania symptoms based on focal brain damage24 August 2020 | Journal of Clinical Investigation, Vol. 130, No. 10Journal of Neuroscience Research, Vol. 96, No. 7 Volume 29Issue 4 Fall 2017Pages 401-408 Metrics KeywordsThalamusMania (Neuropsychiatric Aspects)peduncular hallucinosispsychotic disorderbipolar disorderPDF download History Received 14 November 2016 Accepted 12 December 2016 Published online 15 March 2017 Published in print 1 October 2017