Current Biology Vol 24 No 21 R1026
Essay
Nobel Prize centenary: Robert Bárány and the vestibular system The hundredth anniversary of Robert Bárány’s Nobel Prize in Medicine offers the opportunity to highlight the importance of his discoveries on the physiology and pathophysiology of the vestibular organs. Bárány developed the method of caloric vestibular stimulation that revolutionized the investigation of the semicircular canals and that is still widely used today. Caloric vestibular stimulation launched experimental vestibular research that was relevant to comprehend the evolution of human locomotion, and Bárány’s tests continue to be used in neuroscience to understand the influence of vestibular signals on bodily perceptions, cognition and emotions. Only during the last 20 years has caloric vestibular stimulation been merged with brain imaging to localize the human vestibular cortex. Christophe Lopez1 and Olaf Blanke2,3,4 In 1914, the Austro-Hungarian otologist Robert Bárány (1876–1936) was awarded the Nobel Prize in Medicine “for his work on the physiology and pathology of the vestibular apparatus” (Figure 1). He championed the development and application of new tools for studying the balance system of the inner ear and the oculomotor system [1]. When he won the Nobel prize, Bárány was in a prisoner-of-war camp in Russia; he was only released to receive the award in 1916, after the personal intervention of Prince Carl of Sweden. Prior to the work of Bárány, the anatomy of the inner ear had been well described by Antonio Scarpa and Gustav Retzius — the vestibular organs comprise three semicircular canals and two otolithic organs, the utricule and the saccule (Figure 2A) [2] — but it was not known how head rotations were encoded by the sensory organs of the inner ear, and it was here that Bárány made his key contributions. Bárány was a trained otologist, familiar with the pioneering work on the vestibular system in the 19th century by Pierre Flourens (1794– 1867), Jan Purkinje (1787–1869), Prosper Menière (1799–1862) and Friedrich Goltz (1834–1902). These vestibular pioneers established relations between the semicircular canals and body posture, dizziness and vertigo by observing the consequences of experimental destructions, pathologies, or stimulation of the semicircular canals, but failed to understand their physiology. Further progress was
made in the 1870s by Josef Breuer, Ernst Mach and Alexander Crum Brown, who suggested that the liquid that was filling the semicircular canals was directly involved in self-motion perception. Yet Bárány was the first to comprehend that, by injecting cold and warm water into the auditory canal, the physiology, function and diseases of the vestibular organs could be systematically investigated. Bárány discovered the principles of the caloric test when he was a young otologist in Vienna. He found that, while he was injecting warm and cold water in the auditory canal, subjects reported vertigo and dizziness. Importantly, he described in several articles how such irrigations evoked highly predictable reflexive eye movements, called nystagmus, and that the direction of this ‘caloric nystagmus’ depended on the water’s temperature. Because water at body temperature induced neither vertigo nor eye movements, and because head position changed the direction of the caloric nystagmus, Bárány concluded that the temperature of the water was responsible for stimulation of the semicircular canals in the inner ear and proposed “that the nystagmus was the result of a reflex action of the semicircular canals” [1]. Bárány was the first to understand that warm and cold irrigations of the auditory canal created convection movements of the endolymphatic fluid in the semicircular canals and thereby activated the inner ear’s motion sensors. It has since been confirmed by electrophysiological investigations that warm irrigation creates convection movements that lead mechanoreceptors to increase their
Figure 1. Robert Bárány (1876–1936). Photograph from the US National Library of Medicine.
discharge rate in vestibular afferents, whereas cold irrigation induces the opposite effect (Figure 2B). Bárány’s method revolutionized understanding of the vestibular system, and spurred new experimental vestibular research, such as investigations into the structure of the semicircular canals, that was important for understanding posture and locomotion in animals and humans. As an example, semicircular canals are present in all vertebrates but vary in their form and structure depending on the species’ locomotor behaviour. Analysis of the fine structure of the inner ear of several mammalian species revealed that the size of the semicircular canals is correlated with the agility and range of the animal’s movements [3]. To give another example, stimulation of the semicircular canals in animals (not necessarily based on caloric vestibular stimulation) has also led to the description of neural coding of head motion in central vestibular structures located in the brainstem, cerebellum, thalamus, and the cortex [4]. More recently, Bárány’s caloric test has again become a widely employed research tool for studying
Magazine R1027
the vestibular system, and in particular the vestibular cortex in humans. Neuroimaging techniques such as functional MRI require that subjects keep their head immobile in the scanner, preventing the use of natural vestibular stimulation such as head rotations and translations on motion platforms. Bárány’s caloric stimulation circumvents this problem, is compatible with brain imaging, and has been used over the last 20 years in many modern neuroimaging studies to describe cortical vestibular processing [5,6] in a large network of at least ten cortical areas, including the insula, temporo-parietal junction, intraparietal sulcus, somatosensory cortex, hippocampus and frontal cortex [7]. The location of these vestibular cortical areas seems consistent across primates species, with a core region in the posterior insula, retroinsular cortex and parietal operculum [8] (Figure 2C). Robert Bárány’s discovery was also of major clinical importance as Bárány himself convincingly demonstrated. Bárány’s caloric test is still part of routine assessments of the vestibular system by neuro-otologists, as the absence of caloric nystagmus is indicative of a defective vestibular apparatus. Of note, the caloric test has the advantage to assess the function of the right and left semicircular canals independently. Only recently has a method been developed to evaluate otolith function. Vestibular-evoked myogenic potentials record muscular activity evoked by the stimulation of otolithic receptors by sounds or vibrations [9] and allow quantification of the fundamental vestibular function related to encoding linear accelerations and Earth’s gravitational acceleration. Bárány’s caloric test has also been employed by cognitive neuroscientists to evaluate the impact of vestibular stimulation on a range of perceptual, cognitive and affective processes [10]. Neurologists made extensive use of caloric vestibular stimulation to modify bodily perception and bodily experience in brain-damaged patients. Interestingly, caloric stimulation temporarily alleviates disorders of tactile perception (hemianesthesia), awareness of bodily deficits (anosognosia for hemiplegia, somatoparaphrenia), and chronic pain [5]. The effects and mechanisms of vestibular stimulation on these processes are the subject of intense
A
C TPJ P h
a
OP
Vestibular nerve
u s Cochlea
Eardrum
Insula
B
Gravity
Gravity
Caloric stimulation
Warm caloric stimulation
Cold caloric stimulation Current Biology
Figure 2. The vestibular organs and the caloric test. (A) The inner ear located in the temporal bone. Vestibular organs are formed by three semicircular canals (h: horizontal, a: anterior, and p: posterior canals) coding angular accelerations and by the utricule (u) and saccule (s) encoding horizontal and vertical linear accelerations, respectively. Reproduced from Day and Fitzpatrick [2]. (B) Mechanism of the caloric test. The usual head position for caloric vestibular testing brings the horizontal semicircular canals in a roughly vertical plane. For example, when the right horizontal semicircular canal is positioned vertically while the auditory canal is irrigated with warm water (40°C), convection currents are created in the endolymphatic fluid filling the canal, stimulating the sensory hair cells of the neuroepithelium located in the ampulla of the canal. The mechanoelectrical transduction by the sensory hair cells increases the firing discharge in the vestibular afferents. The opposite effect is evoked by irrigation of the right auditory canal with cold (20°C) water, thus decreasing the firing discharge in the vestibular afferents. (C) Human vestibular cortex identified by caloric vestibular stimulations. Orange areas show vestibular areas identified using a coordinatebased activation likelihood estimation meta-analysis of neuroimaging data. Main vestibular areas are located in the lateral sulcus at the junction of the temporal and parietal cortex (TPJ: temporo-parietal junction), parietal operculum (OP) and insular cortex.
current research [11]. The current view is that vestibular signals modulate the integration of multisensory signals within a large network of cortical and subcortical regions for perception, bodily awareness, and human selfconsciousness [12]. Caloric vestibular stimulation also modulates cognitive functions such as memory and decision-making as well as emotions, mood and affective control [13,14]. Primates and other fast and agile mammals have developed larger semicircular canals (relative to their body mass) and it is known that larger canals increase vestibular sensitivity. Accordingly, it has been proposed that the apparition of human bipedalism and modern humans may be fundamentally associated to the evolution of the structure and function of the inner ear. Human fossils of bipedal Homo erectus have larger vertical semicircular canals
(monitoring head movements for biped locomotion) than horizontal semicircular canals — a pattern not found in other primate species and non-biped hominids [15]. Robert Bárány’s discoveries thus continue to influence vestibular research across many fields of biology, ranging from vestibular physiology to systems and cognitive neuroscience, to consciousness studies and to human evolution, much in the spirit of his native Vienna in the early 20th century. Acknowledgements The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/20072013) under REA grant agreement number 333607. Olaf Blanke is supported by the Swiss National Science Foundation, by the European FP7 project VERE (257695), and the Bertarelli Foundation.
Current Biology Vol 24 No 21 R1028
References
1. Robert Bárány — Nobel Lecture: Some New Methods for Functional Testing of the Vestibular Apparatus and the Cerebellum. Nobelprize.org. Nobel Media AB 2014. Nobelprize.org. Available at: . 2. Day, B.L., and Fitzpatrick, R.C. (2005). The vestibular system. Curr. Biol. 15, R583–R586. 3. Spoor, F., Garland, T., Jr, Krovitz, G., Ryan, T.M., Silcox, M.T., and Walker, A. (2007). The primate semicircular canal system and locomotion. Proc. Natl. Acad. Sci. USA 104, 10808–10812. 4. Angelaki, D.E., and Cullen, K.E. (2008). Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150. 5. Bottini, G., Paulesu, E., Sterzi, R., Warburton, E., Wise, R.J., Vallar, G., Frackowiak, R. S., and Frith, C.D. (1995). Modulation of conscious experience by peripheral sensory stimuli. Nature 376, 778–781. 6. Dieterich, M., Bense, S., Lutz, S., Drzezga, A., Stephan, T., Bartenstein, P., and Brandt, T. (2003). Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb. Cortex 13, 994–1007. 7. Lopez, C., and Blanke, O. (2011). The thalamocortical vestibular system in animals and humans. Brain Res. Rev. 67, 119–146. 8. Grüsser, O.J., Guldin, W.O., Mirring, S., and Salah-Eldin, A. (1994). Comparative physiological and anatomical studies of the primate vestibular cortex. In Structural and Functional Organization of the Neocortex, B. Albowitz, K. Albus, U. Kuhnt, H.C. Nothdurf, and P. Wahle, eds. (Berlin: Springer-Verlag), pp. 358–371. 9. Rosengren, S.M., and Kingma, H. (2013). New perspectives on vestibular evoked myogenic potentials. Curr. Opin. Neurol. 26, 74–80. 10. Miller, S.M., and Ngo, T.T. (2007). Studies of caloric vestibular stimulation: implications for cognitive neurosciences, the clinical neurosciences and neurophilosophy. Acta. Neuropsychiatr. 19, 183–203. 11. Ferrè, E.R., Bottini, G., Iannetti, G.D., and Haggard, P. (2013). The balance of feelings: vestibular modulation of bodily sensations. Cortex 49, 748–758. 12. Blanke, O. (2012). Multisensory brain mechanisms of bodily self-consciousness. Nat. Rev. Neurosci. 13, 556–571. 13. McKay, R., Tamagni, C., Palla, A., Krummenacher, P., Hegemann, S.C.A., Straumann, D., and Brugger, P. (2013). Vestibular stimulation attenuates unrealistic optimism. Cortex 49, 2272–2275. 14. Preuss, N., Hasler, G., and Mast, F.W. (2014). Caloric vestibular stimulation modulates affective control and mood. Brain Stimulat. 7, 133–140. 15. Spoor, F., Wood, B., and Zonneveld, F. (1994). Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369, 645–648. 1Aix
Marseille Université, Centre National de la Recherche Scientifique, NIA UMR 7260, 13331 Marseille, France. 2Center for Neuroprosthetics, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland. 3Laboratory of Cognitive Neuroscience, Brain-Mind Institute, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland. 4Department of Neurology, University Hospital Geneva, 1205 Geneva, Switzerland. E-mail: [email protected], [email protected]
Q&A
Ronald R. Hoy Ron Hoy was an undergraduate at Whitman College and Washington State University, where he majored in Zoology and Psychology. His graduate studies were done at Stanford University, majoring in Biology, followed by a Ph.D. in neurophysiology in Donald Kennedy’s laboratory (1969). He did a postdoc with David Bentley, at Berkeley, on the neurogenetics of cricket songs. His first faculty position in 1971 was at Stony Brook University and he moved to Cornell University 1973 to the Department of Neurobiology and Behavior, where he has remained since and where he is the David and Dorothy Merksamer Professor of Biology and an HHMI Professor. He spent many summers at the Marine Biological Laboratory, where he directed the Neural Systems and Behavior course, and was involved in the Grass Foundation Summer Fellows Program. His career has focused on the neuroethology and bioacoustics of insect songs. His laboratory has investigated the ultrasound-mediated interaction between bats and flying insects, the neuromechanical basis of sound localization in miniscule auditory organs, and the diversity of hearing organs in insects and spiders. His personal interests are in comparative and evolutionary cognitive neuroscience, including music cognition, especially the relationship between language and music. His laboratory has turned to the integration between acoustic and visual signals as part of a program in multimodal, crosssensory integration in the brain. What turned you on to biology in the first place? Even though none of my family was even remotely involved in science, I always found it fascinating. I raised tropical fish in primary school, but even then my obsession was rocketry. I was also an avid reader of Scientific American magazine, where I found a recipe for rocket fuel. I bought zinc powder, sulfur, aluminium dust, and potassium nitrate from farm stores for rocket fuel, and plumbing shops had all I needed for the rocket body. Such efforts resulted in my independently re-inventing the
pipe bomb. My friends and I survived a dozen failed rocket ‘lift-offs’ and eventually I pursued something safer, like brain surgery. And what drew you to a career in bioacoustics and animal behaviour? I have always loved music of all kinds. So it was easy for me to include animal music, the calls of birds, frogs, and insects. This predisposed me to follow bioacoustics. In school lab practicals I was good at dissection, a skill necessary for physiological recording. I combined both bioacoustics and neurobiology when I started my academic career, near the beginning of the golden age of neuroethology (ca. 1970). Recently, my lab has branched out to the visual system of insects and spiders so we can investigate the neuroethology of acousticovisual communication. Acts of social communication demand integration of all the senses! Silent movies were wonderful, but talkies made them immersive. If you had to choose a different field of biology, what would it be? Assuming that we’re talking about a contemporaneous career reboot I’d choose evolutionary microbiology because it’s a whole new take on coevolutionary biology — the world of microbiomes is fascinating. It’s clear that microbiota can alter host behavior — Shelly Adamo’s wonderful work at Dalhousie on host manipulation by pathogens is a great example. What about influences at school? I had wonderful teacher-mentors (see below) who were inspiring lecturers. For all the noise and hype these days about active learning and flipping classrooms — teaching practices that I sometimes apply in my own teaching — I’d hate to see the lecture completely side-lined from the classroom. I don’t think we realize how inspirational and powerful even one lecture can be to a student: a whole new world can be opened up for a student in a mere 50 minutes. There is a social element in human learning and we all love well-told stories. Who were your most influential teachers? In college at Washington State, my physiology teacher Len Kirschner brought me into his lab for my first taste of research — on sodium pumps. In graduate school at Stanford,
Essay
Nobel Prize centenary: Robert Bárány and the vestibular system The hundredth anniversary of Robert Bárány’s Nobel Prize in Medicine offers the opportunity to highlight the importance of his discoveries on the physiology and pathophysiology of the vestibular organs. Bárány developed the method of caloric vestibular stimulation that revolutionized the investigation of the semicircular canals and that is still widely used today. Caloric vestibular stimulation launched experimental vestibular research that was relevant to comprehend the evolution of human locomotion, and Bárány’s tests continue to be used in neuroscience to understand the influence of vestibular signals on bodily perceptions, cognition and emotions. Only during the last 20 years has caloric vestibular stimulation been merged with brain imaging to localize the human vestibular cortex. Christophe Lopez1 and Olaf Blanke2,3,4 In 1914, the Austro-Hungarian otologist Robert Bárány (1876–1936) was awarded the Nobel Prize in Medicine “for his work on the physiology and pathology of the vestibular apparatus” (Figure 1). He championed the development and application of new tools for studying the balance system of the inner ear and the oculomotor system [1]. When he won the Nobel prize, Bárány was in a prisoner-of-war camp in Russia; he was only released to receive the award in 1916, after the personal intervention of Prince Carl of Sweden. Prior to the work of Bárány, the anatomy of the inner ear had been well described by Antonio Scarpa and Gustav Retzius — the vestibular organs comprise three semicircular canals and two otolithic organs, the utricule and the saccule (Figure 2A) [2] — but it was not known how head rotations were encoded by the sensory organs of the inner ear, and it was here that Bárány made his key contributions. Bárány was a trained otologist, familiar with the pioneering work on the vestibular system in the 19th century by Pierre Flourens (1794– 1867), Jan Purkinje (1787–1869), Prosper Menière (1799–1862) and Friedrich Goltz (1834–1902). These vestibular pioneers established relations between the semicircular canals and body posture, dizziness and vertigo by observing the consequences of experimental destructions, pathologies, or stimulation of the semicircular canals, but failed to understand their physiology. Further progress was
made in the 1870s by Josef Breuer, Ernst Mach and Alexander Crum Brown, who suggested that the liquid that was filling the semicircular canals was directly involved in self-motion perception. Yet Bárány was the first to comprehend that, by injecting cold and warm water into the auditory canal, the physiology, function and diseases of the vestibular organs could be systematically investigated. Bárány discovered the principles of the caloric test when he was a young otologist in Vienna. He found that, while he was injecting warm and cold water in the auditory canal, subjects reported vertigo and dizziness. Importantly, he described in several articles how such irrigations evoked highly predictable reflexive eye movements, called nystagmus, and that the direction of this ‘caloric nystagmus’ depended on the water’s temperature. Because water at body temperature induced neither vertigo nor eye movements, and because head position changed the direction of the caloric nystagmus, Bárány concluded that the temperature of the water was responsible for stimulation of the semicircular canals in the inner ear and proposed “that the nystagmus was the result of a reflex action of the semicircular canals” [1]. Bárány was the first to understand that warm and cold irrigations of the auditory canal created convection movements of the endolymphatic fluid in the semicircular canals and thereby activated the inner ear’s motion sensors. It has since been confirmed by electrophysiological investigations that warm irrigation creates convection movements that lead mechanoreceptors to increase their
Figure 1. Robert Bárány (1876–1936). Photograph from the US National Library of Medicine.
discharge rate in vestibular afferents, whereas cold irrigation induces the opposite effect (Figure 2B). Bárány’s method revolutionized understanding of the vestibular system, and spurred new experimental vestibular research, such as investigations into the structure of the semicircular canals, that was important for understanding posture and locomotion in animals and humans. As an example, semicircular canals are present in all vertebrates but vary in their form and structure depending on the species’ locomotor behaviour. Analysis of the fine structure of the inner ear of several mammalian species revealed that the size of the semicircular canals is correlated with the agility and range of the animal’s movements [3]. To give another example, stimulation of the semicircular canals in animals (not necessarily based on caloric vestibular stimulation) has also led to the description of neural coding of head motion in central vestibular structures located in the brainstem, cerebellum, thalamus, and the cortex [4]. More recently, Bárány’s caloric test has again become a widely employed research tool for studying
Magazine R1027
the vestibular system, and in particular the vestibular cortex in humans. Neuroimaging techniques such as functional MRI require that subjects keep their head immobile in the scanner, preventing the use of natural vestibular stimulation such as head rotations and translations on motion platforms. Bárány’s caloric stimulation circumvents this problem, is compatible with brain imaging, and has been used over the last 20 years in many modern neuroimaging studies to describe cortical vestibular processing [5,6] in a large network of at least ten cortical areas, including the insula, temporo-parietal junction, intraparietal sulcus, somatosensory cortex, hippocampus and frontal cortex [7]. The location of these vestibular cortical areas seems consistent across primates species, with a core region in the posterior insula, retroinsular cortex and parietal operculum [8] (Figure 2C). Robert Bárány’s discovery was also of major clinical importance as Bárány himself convincingly demonstrated. Bárány’s caloric test is still part of routine assessments of the vestibular system by neuro-otologists, as the absence of caloric nystagmus is indicative of a defective vestibular apparatus. Of note, the caloric test has the advantage to assess the function of the right and left semicircular canals independently. Only recently has a method been developed to evaluate otolith function. Vestibular-evoked myogenic potentials record muscular activity evoked by the stimulation of otolithic receptors by sounds or vibrations [9] and allow quantification of the fundamental vestibular function related to encoding linear accelerations and Earth’s gravitational acceleration. Bárány’s caloric test has also been employed by cognitive neuroscientists to evaluate the impact of vestibular stimulation on a range of perceptual, cognitive and affective processes [10]. Neurologists made extensive use of caloric vestibular stimulation to modify bodily perception and bodily experience in brain-damaged patients. Interestingly, caloric stimulation temporarily alleviates disorders of tactile perception (hemianesthesia), awareness of bodily deficits (anosognosia for hemiplegia, somatoparaphrenia), and chronic pain [5]. The effects and mechanisms of vestibular stimulation on these processes are the subject of intense
A
C TPJ P h
a
OP
Vestibular nerve
u s Cochlea
Eardrum
Insula
B
Gravity
Gravity
Caloric stimulation
Warm caloric stimulation
Cold caloric stimulation Current Biology
Figure 2. The vestibular organs and the caloric test. (A) The inner ear located in the temporal bone. Vestibular organs are formed by three semicircular canals (h: horizontal, a: anterior, and p: posterior canals) coding angular accelerations and by the utricule (u) and saccule (s) encoding horizontal and vertical linear accelerations, respectively. Reproduced from Day and Fitzpatrick [2]. (B) Mechanism of the caloric test. The usual head position for caloric vestibular testing brings the horizontal semicircular canals in a roughly vertical plane. For example, when the right horizontal semicircular canal is positioned vertically while the auditory canal is irrigated with warm water (40°C), convection currents are created in the endolymphatic fluid filling the canal, stimulating the sensory hair cells of the neuroepithelium located in the ampulla of the canal. The mechanoelectrical transduction by the sensory hair cells increases the firing discharge in the vestibular afferents. The opposite effect is evoked by irrigation of the right auditory canal with cold (20°C) water, thus decreasing the firing discharge in the vestibular afferents. (C) Human vestibular cortex identified by caloric vestibular stimulations. Orange areas show vestibular areas identified using a coordinatebased activation likelihood estimation meta-analysis of neuroimaging data. Main vestibular areas are located in the lateral sulcus at the junction of the temporal and parietal cortex (TPJ: temporo-parietal junction), parietal operculum (OP) and insular cortex.
current research [11]. The current view is that vestibular signals modulate the integration of multisensory signals within a large network of cortical and subcortical regions for perception, bodily awareness, and human selfconsciousness [12]. Caloric vestibular stimulation also modulates cognitive functions such as memory and decision-making as well as emotions, mood and affective control [13,14]. Primates and other fast and agile mammals have developed larger semicircular canals (relative to their body mass) and it is known that larger canals increase vestibular sensitivity. Accordingly, it has been proposed that the apparition of human bipedalism and modern humans may be fundamentally associated to the evolution of the structure and function of the inner ear. Human fossils of bipedal Homo erectus have larger vertical semicircular canals
(monitoring head movements for biped locomotion) than horizontal semicircular canals — a pattern not found in other primate species and non-biped hominids [15]. Robert Bárány’s discoveries thus continue to influence vestibular research across many fields of biology, ranging from vestibular physiology to systems and cognitive neuroscience, to consciousness studies and to human evolution, much in the spirit of his native Vienna in the early 20th century. Acknowledgements The research leading to these results has received funding from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme (FP7/20072013) under REA grant agreement number 333607. Olaf Blanke is supported by the Swiss National Science Foundation, by the European FP7 project VERE (257695), and the Bertarelli Foundation.
Current Biology Vol 24 No 21 R1028
References
1. Robert Bárány — Nobel Lecture: Some New Methods for Functional Testing of the Vestibular Apparatus and the Cerebellum. Nobelprize.org. Nobel Media AB 2014. Nobelprize.org. Available at: . 2. Day, B.L., and Fitzpatrick, R.C. (2005). The vestibular system. Curr. Biol. 15, R583–R586. 3. Spoor, F., Garland, T., Jr, Krovitz, G., Ryan, T.M., Silcox, M.T., and Walker, A. (2007). The primate semicircular canal system and locomotion. Proc. Natl. Acad. Sci. USA 104, 10808–10812. 4. Angelaki, D.E., and Cullen, K.E. (2008). Vestibular system: the many facets of a multimodal sense. Annu. Rev. Neurosci. 31, 125–150. 5. Bottini, G., Paulesu, E., Sterzi, R., Warburton, E., Wise, R.J., Vallar, G., Frackowiak, R. S., and Frith, C.D. (1995). Modulation of conscious experience by peripheral sensory stimuli. Nature 376, 778–781. 6. Dieterich, M., Bense, S., Lutz, S., Drzezga, A., Stephan, T., Bartenstein, P., and Brandt, T. (2003). Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb. Cortex 13, 994–1007. 7. Lopez, C., and Blanke, O. (2011). The thalamocortical vestibular system in animals and humans. Brain Res. Rev. 67, 119–146. 8. Grüsser, O.J., Guldin, W.O., Mirring, S., and Salah-Eldin, A. (1994). Comparative physiological and anatomical studies of the primate vestibular cortex. In Structural and Functional Organization of the Neocortex, B. Albowitz, K. Albus, U. Kuhnt, H.C. Nothdurf, and P. Wahle, eds. (Berlin: Springer-Verlag), pp. 358–371. 9. Rosengren, S.M., and Kingma, H. (2013). New perspectives on vestibular evoked myogenic potentials. Curr. Opin. Neurol. 26, 74–80. 10. Miller, S.M., and Ngo, T.T. (2007). Studies of caloric vestibular stimulation: implications for cognitive neurosciences, the clinical neurosciences and neurophilosophy. Acta. Neuropsychiatr. 19, 183–203. 11. Ferrè, E.R., Bottini, G., Iannetti, G.D., and Haggard, P. (2013). The balance of feelings: vestibular modulation of bodily sensations. Cortex 49, 748–758. 12. Blanke, O. (2012). Multisensory brain mechanisms of bodily self-consciousness. Nat. Rev. Neurosci. 13, 556–571. 13. McKay, R., Tamagni, C., Palla, A., Krummenacher, P., Hegemann, S.C.A., Straumann, D., and Brugger, P. (2013). Vestibular stimulation attenuates unrealistic optimism. Cortex 49, 2272–2275. 14. Preuss, N., Hasler, G., and Mast, F.W. (2014). Caloric vestibular stimulation modulates affective control and mood. Brain Stimulat. 7, 133–140. 15. Spoor, F., Wood, B., and Zonneveld, F. (1994). Implications of early hominid labyrinthine morphology for evolution of human bipedal locomotion. Nature 369, 645–648. 1Aix
Marseille Université, Centre National de la Recherche Scientifique, NIA UMR 7260, 13331 Marseille, France. 2Center for Neuroprosthetics, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland. 3Laboratory of Cognitive Neuroscience, Brain-Mind Institute, École Polytechnique Fédérale de Lausanne, 1015 Lausanne, Switzerland. 4Department of Neurology, University Hospital Geneva, 1205 Geneva, Switzerland. E-mail: [email protected], [email protected]
Q&A
Ronald R. Hoy Ron Hoy was an undergraduate at Whitman College and Washington State University, where he majored in Zoology and Psychology. His graduate studies were done at Stanford University, majoring in Biology, followed by a Ph.D. in neurophysiology in Donald Kennedy’s laboratory (1969). He did a postdoc with David Bentley, at Berkeley, on the neurogenetics of cricket songs. His first faculty position in 1971 was at Stony Brook University and he moved to Cornell University 1973 to the Department of Neurobiology and Behavior, where he has remained since and where he is the David and Dorothy Merksamer Professor of Biology and an HHMI Professor. He spent many summers at the Marine Biological Laboratory, where he directed the Neural Systems and Behavior course, and was involved in the Grass Foundation Summer Fellows Program. His career has focused on the neuroethology and bioacoustics of insect songs. His laboratory has investigated the ultrasound-mediated interaction between bats and flying insects, the neuromechanical basis of sound localization in miniscule auditory organs, and the diversity of hearing organs in insects and spiders. His personal interests are in comparative and evolutionary cognitive neuroscience, including music cognition, especially the relationship between language and music. His laboratory has turned to the integration between acoustic and visual signals as part of a program in multimodal, crosssensory integration in the brain. What turned you on to biology in the first place? Even though none of my family was even remotely involved in science, I always found it fascinating. I raised tropical fish in primary school, but even then my obsession was rocketry. I was also an avid reader of Scientific American magazine, where I found a recipe for rocket fuel. I bought zinc powder, sulfur, aluminium dust, and potassium nitrate from farm stores for rocket fuel, and plumbing shops had all I needed for the rocket body. Such efforts resulted in my independently re-inventing the
pipe bomb. My friends and I survived a dozen failed rocket ‘lift-offs’ and eventually I pursued something safer, like brain surgery. And what drew you to a career in bioacoustics and animal behaviour? I have always loved music of all kinds. So it was easy for me to include animal music, the calls of birds, frogs, and insects. This predisposed me to follow bioacoustics. In school lab practicals I was good at dissection, a skill necessary for physiological recording. I combined both bioacoustics and neurobiology when I started my academic career, near the beginning of the golden age of neuroethology (ca. 1970). Recently, my lab has branched out to the visual system of insects and spiders so we can investigate the neuroethology of acousticovisual communication. Acts of social communication demand integration of all the senses! Silent movies were wonderful, but talkies made them immersive. If you had to choose a different field of biology, what would it be? Assuming that we’re talking about a contemporaneous career reboot I’d choose evolutionary microbiology because it’s a whole new take on coevolutionary biology — the world of microbiomes is fascinating. It’s clear that microbiota can alter host behavior — Shelly Adamo’s wonderful work at Dalhousie on host manipulation by pathogens is a great example. What about influences at school? I had wonderful teacher-mentors (see below) who were inspiring lecturers. For all the noise and hype these days about active learning and flipping classrooms — teaching practices that I sometimes apply in my own teaching — I’d hate to see the lecture completely side-lined from the classroom. I don’t think we realize how inspirational and powerful even one lecture can be to a student: a whole new world can be opened up for a student in a mere 50 minutes. There is a social element in human learning and we all love well-told stories. Who were your most influential teachers? In college at Washington State, my physiology teacher Len Kirschner brought me into his lab for my first taste of research — on sodium pumps. In graduate school at Stanford,
