|Year : 2017 | Volume
| Issue : 1 | Page : 11-15
Understanding the links between vestibular and limbic systems regulating emotions
Archana Rajagopalan1, KV Jinu2, Kumar Sai Sailesh2, Soumya Mishra3, Udaya Kumar Reddy4, Joseph Kurien Mukkadan5
1 Department of Physiology, Saveetha Medical College, Saveetha University, Chennai, Tamil Nadu, India
2 Department of Physiology, Little Flower Institute of Medical Sciences and Research, Angamaly, Kerala, India
3 Department of Physiology, Jawaharlal Institute of Postgraduate Medical Education and Research, Puducherry, India
4 International Stress Management Association-India, Hyderabad, Telangana, India
5 Department of Physiology, Little Flower Medical Research Centre, Angamaly, Kerala, India
|Date of Web Publication||13-Jan-2017|
Joseph Kurien Mukkadan
Department of Physiology, Little Flower Medical Research Centre, Angamaly, Kerala
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Vestibular system, which consists of structures in the inner ear and brainstem, plays a vital role is body balance and patient well-being. In recent years, modulating this system by vestibular stimulation techniques are reported to be effective in stress relief and possibly patient's emotional well-being. Emotions refer to an aroused state involving intense feeling, autonomic activation, and related change in behavior, which accompany many of our conscious experiences. The limbic system is primarily involved in the regulation of emotions. Considering the extensive networks between vestibular and limbic system, it is likely that vestibular stimulation techniques may be useful in influencing emotions. Hence, we review here, the possible mechanisms through which vestibular system can influence emotions and highlight the necessary knowledge gaps, which warrants further research to develop vestibular stimulation techniques as a means to treat health conditions associated with emotional disturbances.
Keywords: Central nervous system and autonomic nervous system, emotions, mental health, vestibular system
|How to cite this article:|
Rajagopalan A, Jinu K V, Sailesh KS, Mishra S, Reddy UK, Mukkadan JK. Understanding the links between vestibular and limbic systems regulating emotions. J Nat Sc Biol Med 2017;8:11-5
|How to cite this URL:|
Rajagopalan A, Jinu K V, Sailesh KS, Mishra S, Reddy UK, Mukkadan JK. Understanding the links between vestibular and limbic systems regulating emotions. J Nat Sc Biol Med [serial online] 2017 [cited 2018 Jan 17];8:11-5. Available from: http://www.jnsbm.org/text.asp?2017/8/1/11/198350
| introduction|| |
Vestibular apparatus located in the inner ear coordinates the body balance and movement, which requires extensive neuronal networking. Vestibular system via the vestibular nuclei has a wide spread of network within the higher centers of the brain, which is evident from the observations of diverse activation patterns following vestibular stimulation. Emotions are aroused state of mind involving intense feeling, autonomic activation, and related change in behavior, which often accompany many of our conscious experiences, including mental and physical components. Vestibular stimulation can modulate mood and hence influence emotions depending on the region of vestibular stimulation. Indeed the concepts of vestibular system influencing emotions has been used therapeutically. For instance, spinning chair was used to treat mania or elevated arousal in nineteenth century. While vestibular dysfunction is well known to affect mood and is associated with anxiety disorders and depression., Conversely, changes in mood/emotions can also influence body balance, which may probably be mediated through vestibulo-ocular reflex pathways.
The influence of vestibular stimulation on emotions is mediated through its projections to limbic system, insula, the cingulate gyre, the hippocampus, and the parabrachial nucleus, via cerebellar, brainstem, diencephalic centers, and amygdale cells.,,,,, Moreover, vestibular system is well-networked with dorsal raphe and the locus coeruleus, which are important structures involved in the regulation of the emotional state., Most of the children and even adults such as movements associated with vestibular stimulation and often show positive emotions following movements leading to vestibular stimulation. Recent research supports using vestibular stimulation as a simple, common therapy for stress-related disorders, which are often difficult to understand and treat with drugs and other conventional therapies., One of the possible mechanisms involved in the benefits from vestibular stimulation may be, reintegration of impaired cortical areas through activating thalamocortical centers. A thorough understand of the mechanisms involved in the benefits from vestibular stimulation are necessary to optimize the therapeutic benefits from these techniques; hence, we review here, the possible mechanisms through which vestibular system can influence emotions.
| Materials and Methods|| |
A detailed review of published literature from Google, PubMed, and MEDLINE was performed and analyzed. The following key words were used in our literature search: vestibular stimulation, mood, and/or emotions.
Vestibular stimulation influences emotions through modulating cerebral cortex
The vestibular nucleus acts as a relay station between the peripheral and central nervous system. Experience and behavior are two major factors, which can influence emotions, and the cerebral cortex plays a critical role in mediating emotions. Both superior and lateral vestibular nuclei have axons networking the ventral posterior nuclear complex of the thalamus, which projects to two cortical areas relevant to the vestibular sensation. Vestibular stimulation was found to modulate brain functions, probably by activating somatosensory areas, (particularly the thalamocortical), and deactivating the visual areas. These studies strongly support the role of the cerebral cortex and the pathways networking the vestibular nuclei in regulating emotions. It is likely that these networks may exist in several forms include the chemical forms (dopamine, serotonin, acetylcholine, and norepinephrine) which are part of the diffused modulatory systems.
Role of limbic system in vestibular stimulation influencing emotions
The limbic system is a major cluster of higher centers, which influences emotions. The limbic system consists of cingulate gyrus and parahippocampal gyrus in the cerebral cortex, several nuclei in the cerebrum, amygdala, hypothalamus (mammillary body), and hippocampus. The anatomical organization of the limbic system varies across different species and is highly developed in species exhibiting strong emotional behaviors. The role of the limbic system in emotion was first explained by James Papez in 1937 in his paper titled “A proposed mechanism of emotion.” The model proposed by him was popularly known as Papez circuit, which highlighted the presence of neuronal pathways between vestibular system and limbic system. Vestibular stimulation activated the limbic system and neocortex; hence, providing a neuroanatomical and probably a neurochemical link between vestibular stimulation and the limbic dopaminergic system., However, our current understanding of these complex neuronal networks is very limited, which warrants further research to decipher the mechanisms by which vestibular stimulation triggers these networks to influence emotions.
The hypothalamus is a vital part of the limbic system; hence, vestibular stimulation by influencing hypothalamus can impact emotions either independently or as part of the general limbic system networks. Indeed, the influence of hypothalamus on emotional behavior is previously reported, which is not surprising considering the role of this center in thermoregulation and several vital endocrine functions. Lesions of hypothalamus are usually associated with extreme passivity, loss of drive/motivation, excessive eating and drinking, and rage and violent behavior. Several of these behaviors are often of extreme social concern both from the patients and societal views. Hence, research to understand the role and utility of simple interventions such as vestibular stimulations to cure such disorders associated with hypothalamus malfunction may be of immense medical benefit. Such research may specifically look at further understanding the role of HPA axis modulation by vestibular stimulation through vestibulo-paraventricular polysynaptic pathways. Interestingly, vestibular system is also connected with lateral and posterior hypothalamus, which has a very diverse endocrine role and necessitates further research to understand the utility of vestibular stimulation in influencing this vital physiology.
Like hypothalamus, amygdale, and hippocampus are also part of the limbic system and hence are involved in the regulation of emotions and probably memory. Specifically, amygdala and prefrontal activity integration are reported to play a key role in the regulation of emotions. Retrograde viral transneuronal tracing has strongly supported the existence of vestibular projections to central amygdala cells, which indicates the possible utility of vestibular stimulation in influencing the physiology of amygdala. Amygdala is also a neural substrate which is involved in the development of and habituation to motion sickness; hence, it is likely that vestibular stimulation may have a role in treating motion sickness disorders and aid in promoting patients quality of life. The interaction of amygdale and hippocampus plays an important role in emotions. It was reported that amygdale can modulate both the encoding and the storage of hippocampal-dependent memories, indicating a potential role for vestibular stimulation techniques in improving memory-related health issues. Further supporting the role for vestibular stimulations in influencing emotions is a presence of anatomical, functional and chemical connections between vestibular nuclei and hippocampus, which can be triggered to activate hippocampus.,,
Vestibular stimulation regulates autonomic nervous system to influence emotions
The activity of autonomic nervous system (ANS) is considered as a major component of peripheral nervous system, which can influence emotional response. Within this, the balancing regulation of sympathetic and parasympathetic systems in influencing several systemic physiology is well known. Vestibular system influences autonomic regulation through vestibule-autonomic networks., Interestingly, autonomic malfunctioning is reported as a probable cause for vertigo  and several other cardiovascular, renovascular, and cerebrovascular disorders. Probably, ANS may be one of the major targets that are positively influenced by vestibular stimulation techniques; hence, the systemic benefits observed with such interventions. Vestibular system balances autonomic activity by stimulating vagal system and inhibiting sympathetic system;,,, hence, driving the physiology toward a much calmer state.
Vestibular stimulation influences emotions through regulating several higher centers in the central nervous system
The insula represents emotional experience because it receives interoceptive inputs from the whole body, and its connections with the prefrontal regions of the cortex can provide contextual information. Activation of the insula was reported to influence subjective feelings, which may involve the inputs from the limbic system networks as highlighted above. Anterior cingulate cortex (ACC) and the medial prefrontal cortex have also long been thought to play a critical role in emotional processing,, either independently or possibly via the limbic networks. Hence, by modulating these higher centers in the central nervous system, vestibular stimulation may positively influence emotions. This is further supported by the core regions of the multimodal vestibular cortex, which is defined as the PIVC.,,,, Anatomical, physiological, and chemical-based vestibular projections exist to anterior insula, adjacent inferior frontal gyrus, and ACC, which has a regulatory role on interoceptive inputs necessary for physiology of emotions.,,,,
The parabrachial nucleus produces somatic, emotional sense in integration with amygdale, and insula. To and fro projections from vestibular nucleus to parabrachial complex were traced in several animal models,,,, which further supports the role for vestibular stimulation in regulating physiology of emotions. Indeed parabrachial nuclear complex containing neurons responsive to vestibular stimulation has been demonstrated.
Dorsal raphe nucleus (DRN) is a major source of serotonin and modulation of serotonin levels, has a major role in value-based decision-making process. Interestingly, serotonin is also a major player in diffuse modulatory systems, which help vestibular nuclei connect with the limbic system and hence regulate emotions. The malfunction of serotonin or its receptors (5-HT system) is associated with several emotional/neuronal disorders such as depression, schizophrenia, drug abuse, autism, and Parkinson's disease. Indeed several direct and indirect connections exist between vestibular nucleus and DRN,,,,, further supporting the role for vestibular stimulation in activating DRN  and regulation of emotions.
| Conclusion|| |
The vestibular system is extensively networked with the limbic system, and hence vestibular stimulation can influence emotional behavior by regulating several higher centers in the central nervous system and autonomic nervous system. A detailed understanding of the anatomy, physiology, and biochemistry of these networks is necessary to refine the therapeutic utility of vestibular stimulation for various medical conditions influencing patient emotions.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev 2011;67:119-46.
Khurana I. Medical Physiology for Undergraduate Students. 1/e. New Delhi: Elsevier, a Division of Reed Elsevier India Private Limited; 2012. p. 851-2.
Preuss N, Hasler G, Mast FW. Caloric vestibular stimulation modulates affective control and mood. Brain Stimul 2014;7:133-40.
Winter L, Wollmer MA, Laurens J, Straumann D, Kruger TH. Cox's chair revisited: Can spinning alter mood states? Front Psychiatry 2013;4:132.
Nagaratnam N, Ip J, Bou-Haidar P. The vestibular dysfunction and anxiety disorder interface: A descriptive study with special reference to the elderly. Arch Gerontol Geriatr 2005;40:253-64.
Best C, Bense S, Dieterich M. Vestibular dysfunction in major depression. Neuroscience 2007;147:865-6.
Bolmont B, Gangloff P, Vouriot A, Perrin PP. Mood states and anxiety influence abilities to maintain balance control in healthy human subjects. Neurosci Lett 2002;329:96-100.
Suzuki M, Kitano H, Ito R, Kitanishi T, Yazawa Y, Ogawa T, et al.
Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Brain Res Cogn Brain Res 2001;12:441-9.
Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, et al.
Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 2002;17:1384-93.
Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al.
Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 2005;26:721-32.
Dieterich M. Functional brain imaging: A window into the visuo-vestibular systems. Curr Opin Neurol 2007;20:12-8.
Lopez C, Blanke O. The thalamocortical vestibular system in animals and humans. Brain Res Rev 2011;67:119-4610.
Metts BA, Kaufman GD, Perachio AA. Polysynaptic inputs to vestibular efferent neurons as revealed by viral transneuronal tracing. Exp Brain Res 2006;172:261-74.
Halberstadt AL, Balaban CD. Anterograde tracing of projections from the dorsal raphe nucleus to the vestibular nuclei. Neuroscience 2006;143:641-54.
Halberstadt AL, Balaban CD. Serotonergic and nonserotonergic neurons in the dorsal raphe nucleus send collateralized projections to both the vestibular nuclei and the central amygdaloid nucleus. Neuroscience 2006;140:1067-77.
Noll-Hussong M, Holzapfel S, Pokorny D, Herberger S. Caloric vestibular stimulation as a treatment for conversion disorder: A case report and medical hypothesis. Front Psychiatry 2014;5:63.
Dodson MJ. Vestibular stimulation in mania: A case report. J Neurol Neurosurg Psychiatry 2004;75:168-9.
Schiff ND, Pulver M. Does vestibular stimulation activate thalamocortical mechanisms that reintegrate impaired cortical regions? Proc Biol Sci 1999;266:421-3.
Heilman KM, Gilmore RL. Cortical influences in emotion. J Clin Neurophysiol 1998;15:409-23.
Purves D, Augustine GJ, Fitzpatrick D, Katz LC, LaMantia AS, McNamara JO, et al
. editors. Neuroscience. 2nd
ed. Sunderland, MA: Sinauer Associates, Inc.; 2001.
Been G, Ngo TT, Miller SM, Fitzgerald PB. The use of tDCS and CVS as methods of non-invasive brain stimulation. Brain Res Rev 2007;56:346-61.
Ferrè ER, Bottini G, Haggard P. Vestibular inputs modulate somatosensory cortical processing. Brain Struct Funct 2012;217:859-64.
Papez JW. A proposed mechanism of emotion. Arch Neurol Psychiatry 1937;38:725-43.
Saman Y, Bamiou DE, Gleeson M, Dutia MB. Interactions between stress and vestibular compensation – A review. Front Neurol 2012;3:116.
Rappaport N, Coffey B. Psychopharmacology in the school setting: Therapeutic challenges in an adolescent with attention deficit hyperactivity disorder, possible bipolar disorder, and other comorbidity. J Child Adolesc Psychopharmacol 2004;14:3-7.
Vitte E, Derosier C, Caritu Y, Berthoz A, Hasboun D, Soulié D. Activation of the hippocampal formation by vestibular stimulation: A functional magnetic resonance imaging study. Exp Brain Res 1996;112:523-6.
Hess WR, Akert K. Experimental data on role of hypothalamus in mechanism of emotional behavior. AMA Arch Neurol Psychiatry 1955;73:127-9.
Markia B, Kovács ZI, Palkovits M. Projections from the vestibular nuclei to the hypothalamic paraventricular nucleus: Morphological evidence for the existence of a vestibular stress pathway in the rat brain. Brain Struct Funct 2008;213:239-45.
Doll A, Hölzel BK, Mulej Bratec S, Boucard CC, Xie X, Wohlschläger AM, et al.
Mindful attention to breath regulates emotions via increased amygdala-prefrontal cortex connectivity. Neuroimage 2016;134:305-13.
Nakagawa A, Uno A, Horii A, Kitahara T, Kawamoto M, Uno Y, et al.
Fos induction in the amygdala by vestibular information during hypergravity stimulation. Brain Res 2003;986:114-23.
Phelps EA. Human emotion and memory: Interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 2004;14:198-202.
Smith PF. Vestibular-hippocampal interactions. Hippocampus 1997;7:465-71.
Hüfner K, Hamilton DA, Kalla R, Stephan T, Glasauer S, Ma J, et al.
Spatial memory and hippocampal volume in humans with unilateral vestibular deafferentation. Hippocampus 2007;17:471-85.
Cuthbert PC, Gilchrist DP, Hicks SL, Mac Dougall HG, Curthoys IS. Electro physiological evidence for vestibular activation of guinea pig hippocampus. Neuroreport 2000;11:1443-7.
Kreibig SD. Autonomic nervous system activity in emotion: A review. Biol Psychol 2010;84:394-421.
Yates BJ, Bronstein AM. The effects of vestibular system lesions on autonomic regulation: Observations, mechanisms, and clinical implications. J Vestib Res 2005;15:119-29.
Furman JM, Jacob RG, Redfern MS. Clinical evidence that the vestibular system participates in autonomic control. J Vestib Res 1998;8:27-34.
Takeda N. Autonomic dysfunction and vertigo. Jpn Med Assoc J 2006;49:153-7.
Porter JD, Balaban CD. Connections between the vestibular nuclei and brain stem regions that mediate autonomic function in the rat. J Vestib Res 1997;7:63-76.
Holstein GR, Friedrich VL Jr., Martinelli GP. Projection neurons of the vestibulo-sympathetic reflex pathway. J Comp Neurol 2014;522:2053-74.
Saini AK, Patel RJ, Sharma SS, Kumar AH. Edaravone attenuates hydroxyl radical stress and augmented angiotensin II response in diabetic rats. Pharmacol Res 2006;54:6-10.
Biaggioni I, Costa F, Kaufmann H. Vestibular influences on autonomic cardiovascular control in humans. J Vestib Res 1998;8:35-41.
Suzuki A. Emotional functions of the insula. Brain Nerve 2012;64:1103-12.
Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci 2011;15:85-93.
Guldin WO, Grüsser OJ. Is there a vestibular cortex? Trends Neurosci 1998;21:254-9.
Brandt T, Dieterich M. The vestibular cortex. Its locations, functions, and disorders. Ann N
Y Acad Sci 1999;871:293-312.
Indovina I, Maffei V, Bosco G, Zago M, Macaluso E, Lacquaniti F. Representation of visual gravitational motion in the human vestibular cortex. Science 2005;308:416-9.
Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 2012;212:159-79.
Clover AJ, Kumar AH, Caplice NM. Deficiency of C×3CR1 delays burn wound healing and is associated with reduced myeloid cell recruitment and decreased sub-dermal angiogenesis. Burns 2011;37:1386-93.
Gu X, Hof PR, Friston KJ, Fan J. Anterior insular cortex and emotional awareness. J Comp Neurol 2013;521:3371-88.
Craig AD. How do you feel – now? The anterior insula and human awareness. Nat Rev Neurosci 2009;10:59-70.
Shinder ME, Taube JS. Differentiating ascending vestibular pathways to the cortex involved in spatial cognition. J Vestib Res Equilib Orientat 2010;20:3-23.
Arun KH, Kaul CL, Poduri R. Tempol augments angiotensin II-induced AT2 receptor-mediated relaxation in diabetic rat thoracic aorta. J Hypertens 2004;22:2143-52.
Hitier M, Besnard S, Smith PF. Vestibular pathways involved in cognition. Front Integr Neurosci 2014;8:59.
Lenhardt ML, Shulman A, Goldstein BA. The role of the parabrachial nucleus in the natural history of tinnitus and its implications. Int Tinnitus J 2007;13:87-9.
Suzuki T, Sugiyama Y, Yates BJ. Integrative responses of neurons in parabrachial nuclei to a nauseogenic gastrointestinal stimulus and vestibular stimulation in vertical planes. Am J Physiol Regul Integr Comp Physiol 2012;302:R965-75.
O'Sullivan JF, Leblond AL, Kelly G, Kumar AH, Metharom P, Büneker CK, et al.
Potent long-term cardioprotective effects of single low-dose insulin-like growth factor-1 treatment postmyocardial infarction. Circ Cardiovasc Interv 2011;4:327-35.
Balaban CD. Projections from the parabrachial nucleus to the vestibular nuclei: Potential substrates for autonomic and limbic influences on vestibular responses. Brain Res 2004;996:126-37.
McCandless CH, Henderson C. Responses of Parabrachial Nucleus Neurons to Whole Body Motion in the Macaque. Doctoral Dissertation; 2007. Available from: http://www.dscholarship.pitt.edu/7819
. [Last accessed on 2016 Apr 13, 9:46 am].
Nakamura K. The role of the dorsal raphé nucleus in reward-seeking behavior. Front Integr Neurosci 2013;7:60.
Horowitz SS, Blanchard J, Morin LP. Medial vestibular connections with the hypocretin (orexin) system. J Comp Neurol 2005;487:127-46.
London LE, Kumar AH, Wall R, Casey PG, O'Sullivan O, Shanahan F, et al.
Exopolysaccharide-producing probiotic Lactobacilli reduce serum cholesterol and modify enteric microbiota in ApoE-deficient mice. J Nutr 2014;144:1956-62.
Snowball RK, Dampney RA, Lumb BM. Responses of neurones in the medullary raphe nuclei to inputs from visceral nociceptors and the ventrolateral periaqueductal grey in the rat. Exp Physiol 1997;82:485-500.
Abols IA, Basbaum AI. Afferent connections of the rostral medulla of the cat: a neural substrate for midbrain-medullary interactions in the modulation of pain. J Comp Neurol 1981;201:285-97.
Basbaum AI, Fields HL. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 1984;7:309-38.