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Regional Brain Responses Associated with Using Imagination to Evoke and Satiate Thirst

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Regional Brain Responses Associated with Using Imagination to Evoke and Satiate Thirst Regional brain responses associated with using imagination to evoke and satiate thirst Pascal Sakera, Steve Careyb, Marcus Grohmannc, Michael J. Farrelld,e,f,1, Philip J. Ryana, Gary F. Egand,f, Michael J. McKinleya,g, and Derek A. Dentona,h,i,1 aFlorey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, VIC 3010, Australia; bSteve Carey Hypnotherapy, Hampton, VIC 3192, Australia; cHygiene Technologie Kompetenzzentrum GmbH, 96049 Bamberg, Germany; dMonash Biomedical Imaging, Monash University, Clayton, VIC 3800, Australia; eDepartment of Medical Imaging and Radiation Sciences, School of Primary and Allied Health Care, Monash University, Clayton, VIC 3800, Australia; fAustralian Research Council Centre of Excellence for Integrative Brain Function, Monash University, Clayton, VIC 3800, Australia; gDepartment of Physiology, University of Melbourne, Parkville, VIC 3010, Australia; hFaculty of Medicine, Dentistry and Health Sciences, University of Melbourne, Parkville, VIC 3010, Australia; and iBaker Heart and Diabetes Institute, Melbourne, VIC 3004, Australia Contributed by Derek A. Denton, April 14, 2020 (sent for review February 14, 2020; reviewed by Michael T. Alkire and Brent Alan Vogt) In response to dehydration, humans experience thirst. This subjective which a significant relationship between thirst ratings and fluid state is fundamental to survival as it motivates drinking, which loss has not been observed (12, 13). We therefore questioned subsequently corrects the fluid deficit. To elicit thirst, previous studies whether a physiological stimulus is indeed necessary for thirst to have manipulated blood chemistry to produce a physiological thirst be experienced. Since the intensity of subjective thirst may not stimulus. In the present study, we investigated whether a physiolog- reflect the underlying fluid deficit, the two phenomena could be ical stimulus is indeed required for thirst to be experienced. Functional dissociable. This raises the possibility that subjective thirst can be MRI (fMRI) was used to scan fully hydrated participants while they evoked while in a fully hydrated state, an outcome that repre- imagined a state of intense thirst and while they imagined drinking to sents a complete dissociation of the conscious experience from satiate thirst. Subjective ratings of thirst were significantly higher for the underlying physiological state. imagining thirst compared with imagining drinking or baseline, Indirect evidence for this possibility has been provided in recent revealing a successful dissociation of thirst from underlying physiol- animal studies in which optogenetic stimulation of thirst-related ogy. The imagine thirst condition activated brain regions similar to neurons in the circumventricular organs produced robust drinking those reported in previous studies of physiologically evoked thirst, behavior in fully satiated mice (14, 15). In these studies, however, NEUROSCIENCE including the anterior midcingulate cortex (aMCC), anterior insula, the experience of thirst could not be confirmed due to our inability precentral gyrus, inferior frontal gyrus, middle frontal gyrus, and to interrogate the subjective state of other species. Since a com- operculum, indicating a similar neural network underlies both imag- parable optogenetic procedure in humans is not feasible, the use ined thirst and physiologically evoked thirst. Analogous brain regions of imagination as a stimulus represents a viable alternative that were also activated during imagined drinking, suggesting the neural has been exploited in several other studies of interoceptive expe- representation of thirst contains a drinking-related component. Finally, riences, including pain (16) and hunger (17). With this approach, theaMCCshowedanincreaseinfunctionalconnectivitywiththe an investigation can be undertaken in humans of subjective thirst insula during imagined thirst relative to imagined drinking, implying functional connectivity between these two regions is needed before and its underlying neural circuitry in the complete absence of a thirst can be experienced. As a result of these findings, this study physiological stimulus. provides important insight into how the neural representation of sub- It is also possible, using this approach, to cue the initiation and jective thirst is generated and how it subsequently motivates termination of imagined thirst. A state of imagined thirst can drinking behavior. consequently be examined using functional MRI (fMRI) and brain thirst | dehydration | cingulate | insula | fMRI Significance uman neuroimaging has revealed a network of brain regions This study provides three important insights into the neural Hassociated with the subjective experience of thirst. These representation of thirst. First, the experience of thirst can be regions include the cingulate cortex, insula, primary sensorimo- dissociated from a physiological stimulus produced by changes tor cortex, inferior frontal gyrus, and middle frontal gyrus (1–8). in blood chemistry. Second, the network of brain regions as- In previous studies, thirst has been evoked with administration of sociated with subjective thirst may incorporate regions involved intravenous (i.v.) hypertonic saline solution (1–4, 6), through in drinking behavior. Third, functional connectivity between water and electrolyte loss caused by exercise-induced sweating the insula and the anterior midcingulate cortex appears (5), and by fluid deprivation (7, 8). These physiological manip- necessary to generate an experience of thirst. In the absence ulations produce changes in osmotic pressure, sodium concen- of a physiological stimulus, use of imagination to evoke thirst tration, and angiotensin II concentration that are detected by also provides a means of investigating this subjective state receptors within the circumventricular organs of the lamina with fMRI. terminalis (9), a region of the brain without a blood–brain barrier Author contributions: P.S., S.C., M.G., M.J.F., P.J.R., G.F.E., M.J.M., and D.A.D. designed (10). The changes in blood composition detected by these re- research; P.S., S.C., and M.G. performed research; P.S. and M.J.F. analyzed data; and P.S., ceptors produce a physiological thirst stimulus, which leads to S.C., M.J.F., P.J.R., G.F.E., M.J.M., and D.A.D. wrote the paper. the generation of a thirst experience. Reviewers: M.T.A., University of California, Irvine; and B.A.V., Boston University School The state of thirst that arises from a physiological stimulus is of Medicine. critical to maintaining homeostasis, and thus survival, because it The authors declare no competing interest. motivates goal-directed drinking. As a result of this behavior, the Published under the PNAS license. fluid deficit produced by dehydration is corrected. While the 1To whom correspondence may be addressed. Email: [email protected] or relationship between physiological stimulus and subjective thirst [email protected]. is clearly important for survival, previous evidence suggests the This article contains supporting information online at https://www.pnas.org/lookup/suppl/ subjective experience is not tightly coupled to the stimulus (11). doi:10.1073/pnas.2002825117/-/DCSupplemental. This inference is supported by previous work from our group, in www.pnas.org/cgi/doi/10.1073/pnas.2002825117 PNAS Latest Articles | 1of7 Downloaded by guest on September 24, 2021 activity associated with imagined thirst and imagined satiation can Imagine be directly compared. The state of thirst produced by a physio- logical stimulus, in contrast, cannot be used in such a comparison Structural as dehydration or infusion of hypertonic saline produces relatively scan Scan 1 Scan 2 slow changes in blood chemistry that are incompatible with the temporal dynamics of fMRI. For the present study, we compared and contrasted brain ac- 10 mins 7.7 mins 7.7 mins tivation in an fMRI block design in which trained hypnosis practitioners, and thus individuals who use their imaginative 4 trials ability regularly, imagined thirst in one condition (“imagine per scan thirst”) and imagined satiating their thirst by drinking in another condition (“imagine drink”). While previous studies have been unable to directly contrast these two states, drinking in response to thirst has been shown to activate a similar network of brain regions as the experience of thirst itself (12, 18). By comparing two subjective states with similar activation patterns but with only one of the states specifically associated with the experience of thirst, we aimed to reveal unique characteristics of the neural Thirst Drink network that underlies the thirst experience. Using a psycho- cue cue physiological interaction (PPI) approach (19, 20), we also aimed to investigate the degree of correlated activity, or functional rang rang Rang connectivity, between brain regions during each of the imagined Fixate cue cue cue conditions to further elucidate and clarify the network un- derlying the experience of thirst. Based on previous reports that have emphasized consistent activation in the anterior mid- 30 7 307 30 7 cingulate cortex (aMCC) with respect to thirst and drinking (18), (secs) the PPI analyses examined functional connectivity between the aMCC and the rest of the brain. Behavioral Results Single trial Mock Scanner. To test whether a thirst experience could indeed be Fig. 1. Experimental protocol composed of one structural scan and two evoked by imagination, each participant initially performed the functional
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