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Influence Of Anterior Midcingulate Cortex On Drinking Behavior During Thirst And Following Satiation

P. Saker, M. Farrell, G. Egan, M. Mckinley, D. Denton
Published 2018 · Medicine

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Significance This study provides important insight into how the human brain regulates fluid intake in response to changes in hydration status. The findings presented here reveal that activity in the anterior midcingulate cortex (aMCC) is associated with drinking responses during a state of thirst, and that this region is likely to contribute to the facilitation of drinking during this state. These results are consistent with a reduction in the influence of the aMCC contributing to the conclusion of drinking during a state of satiation. Because drinking stops before changes in blood volume and chemistry signal the restoration of fluid balance, these results implicate the aMCC in the regulation of drinking behavior before these changes manifest within the circulatory system. In humans, activity in the anterior midcingulate cortex (aMCC) is associated with both subjective thirst and swallowing. This region is therefore likely to play a prominent role in the regulation of drinking in response to dehydration. Using functional MRI, we investigated this possibility during a period of “drinking behavior” represented by a conjunction of preswallow and swallowing events. These events were examined in the context of a thirsty condition and an “oversated” condition, the latter induced by compliant ingestion of excess fluid. Brain regions associated with swallowing showed increased activity for drinking behavior in the thirsty condition relative to the oversated condition. These regions included the cingulate cortex, premotor areas, primary sensorimotor cortices, the parietal operculum, and the supplementary motor area. Psychophysical interaction analyses revealed increased functional connectivity between the same regions and the aMCC during drinking behavior in the thirsty condition. Functional connectivity during drinking behavior was also greater for the thirsty condition relative to the oversated condition between the aMCC and two subcortical regions, the cerebellum and the rostroventral medulla, the latter containing nuclei responsible for the swallowing reflex. Finally, during drinking behavior in the oversated condition, ratings of swallowing effort showed a negative association with functional connectivity between the aMCC and two cortical regions, the sensorimotor cortex and the supramarginal gyrus. The results of this study provide evidence that the aMCC helps facilitate swallowing during a state of thirst and is therefore likely to contribute to the regulation of drinking after dehydration.
This paper references
Dorsal anterior midcingulate cortex : Roles in normal cognition and disruption in attention - deficit / hyperactivity disorder
G Bush (2009)
10.1073/PNAS.0511019103
Unique, common, and interacting cortical correlates of thirst and pain
M. Farrell (2006)
10.1016/j.jchemneu.2016.01.010
Midcingulate cortex: Structure, connections, homologies, functions and diseases
B. Vogt (2016)
10.1523/JNEUROSCI.4597-10.2011
Investigation of the Neural Control of Cough and Cough Suppression in Humans Using Functional Brain Imaging
S. Mazzone (2011)
10.1152/PHYSREV.2001.81.2.929
Brain stem control of swallowing: neuronal network and cellular mechanisms.
A. Jean (2001)
Characteristics of the swallowing reflex induced by peripheral nerve and brain stem stimulation
AJ Miller (1972)
10.1093/MILMED/167.5.432
Death by water intoxication.
J. W. Gardner (2002)
10.1016/0031-9384(84)90154-9
Body fluid changes, thirst and drinking in man during free access to water
P. A. Phillips (1984)
10.1016/j.neuroimage.2008.04.234
Sensory stimulation activates both motor and sensory components of the swallowing system
Soren Y. Lowell (2008)
10.1016/j.schres.2008.09.029
Mortality over a 20-year period in patients with primary polydipsia associated with schizophrenia: A retrospective study
E. Hawken (2009)
10.1073/pnas.2136650100
Neural correlates of the emergence of consciousness of thirst
G. Egan (2003)
10.1007/s00455-009-9211-6
Brain Stem Control of the Phases of Swallowing
I. M. Lang (2009)
10.1152/ajpgi.1999.277.1.G219
Cortical activation during human volitional swallowing: an event-related fMRI study.
S. Hamdy (1999)
10.1152/AJPREGU.1980.239.5.R476
Thirst following water deprivation in humans.
B. Rolls (1980)
10.1073/pnas.012470999
Dorsal anterior cingulate cortex: A role in reward-based decision making
G. Bush (2001)
10.1006/nimg.1999.0459
Three-Dimensional MRI Atlas of the Human Cerebellum in Proportional Stereotaxic Space
J. Schmahmann (1999)
10.1073/PNAS.96.5.2532
Correlation of regional cerebral blood flow and change of plasma sodium concentration during genesis and satiation of thirst.
D. Denton (1999)
10.1007/s00455-007-9080-9
Normal Swallowing and Functional Magnetic Resonance Imaging: A Systematic Review
I. Humbert (2007)
10.1152/JN.2001.85.2.938
Cerebral cortical representation of automatic and volitional swallowing in humans.
R. Martin (2001)
10.1016/0165-1838(82)90003-0
The central projections of the trigeminal, facial, glossopharyngeal and vagus nerves: an autoradiographic study in the rat.
R. J. Contreras (1982)
10.1006/nimg.1997.0291
Psychophysiological and Modulatory Interactions in Neuroimaging
Karl J. Friston (1997)
10.1212/WNL.39.9.1169
Anterior operculum syndrome
Chi-Chen Mao (1989)
10.1002/ddrr.12
The neurobiology of swallowing and dysphagia.
A. Miller (2008)
10.1073/PNAS.040555497
Neuroimaging evidence implicating cerebellum in support of sensory/cognitive processes associated with thirst.
L. Parsons (2000)
10.1007/s002210100813
Parallel cortical networks for volitional control of swallowing in humans
K. Mosier (2001)
10.1007/s00455-010-9301-5
Sensory Input Pathways and Mechanisms in Swallowing: A Review
C. Steele (2010)
10.1073/PNAS.96.9.5304
Neuroimaging of genesis and satiation of thirst and an interoceptor-driven theory of origins of primary consciousness.
D. Denton (1999)
10.1152/AJPGI.00323.2003
Role of primary sensorimotor cortex and supplementary motor area in volitional swallowing: a movement-related cortical potential study.
T. Satow (2004)
Role of cerebral cortex in the control of swallowing. GI Motility Online
S Hamdy (2006)
10.1152/AJPGI.2001.280.3.G354
Cerebral cortical representation of reflexive and volitional swallowing in humans.
M. Kern (2001)
10.1126/science.aan6747
Thirst-associated preoptic neurons encode an aversive motivational drive
W. E. Allen (2017)
10.1007/s00221-004-2048-1
Discrete functional contributions of cerebral cortical foci in voluntary swallowing: a functional magnetic resonance imaging (fMRI) “Go, No-Go” study
Jillian A. Toogood (2004)
10.1073/pnas.1403382111
Regional brain responses associated with drinking water during thirst and after its satiation
P. Saker (2014)
10.1152/JN.00297.2003
Human cortical responses to water in the mouth, and the effects of thirst.
I. D. de Araujo (2003)
10.1016/j.neuroimage.2009.05.030
fMRI in the presence of task-correlated breathing variations
R. Birn (2009)
10.1038/nn.4575
The cellular mechanism for water detection in the mammalian taste system
Dhruv Zocchi (2017)
10.1016/0014-4886(72)90168-9
Characteristics of the swallowing reflex induced by peripheral nerve and brain stem stimulation.
A. Miller (1972)
10.1097/MOO.0b013e32832b255e
Cortical input in control of swallowing
E. Michou (2009)
10.3389/fnhum.2017.00234
From Thirst to Satiety: The Anterior Mid-Cingulate Cortex and Right Posterior Insula Indicate Dynamic Changes in Incentive Value
C. Becker (2017)
10.1002/CNE.901930211
Brain stem projections of sensory and motor components of the vagus complex in the cat: II. Laryngeal, tracheobronchial, pulmonary, cardiac, and gastrointestinal branches
M. Kalia (1980)
Dorsal anterior midcingulate cortex: Roles in normal cognition and disruption in attention-deficit/hyperactivity disorder. Cingulate Neurobiology and Disease, ed Vogt BA (Oxford
G Bush (2009)
10.1016/S0031-9384(99)00210-3
The role of mouth state in the termination of drinking behavior in humans
J. Brunstrom (2000)
10.1093/CHEMSE/25.3.267
Cortical activation induced by intraoral stimulation with water in humans.
D. Zald (2000)
10.1002/CNE.901060104
Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. An experimental study in the rat
A. Torvik (1956)
10.1093/brain/aws186
Mapping motor representations in the human cerebellum.
C. Mottolese (2013)
Dorsal Anterior Midcingulate Cortex: Roles in Normal Cognition and Disruption in Attention-Defi cit/ Hyperactivity Disorder
G. Bush (2015)
10.1002/hbm.20680
Functional brain imaging of swallowing: An activation likelihood estimation meta‐analysis
Peter Sörös (2009)
10.1038/nn1354
Human anterior cingulate neurons and the integration of monetary reward with motor responses
Z. Williams (2004)
10.1093/scan/nss055
Tools of the trade: psychophysiological interactions and functional connectivity.
J. O’Reilly (2012)
10.1152/ajpregu.00817.2010
Cortical activation and lamina terminalis functional connectivity during thirst and drinking in humans.
M. Farrell (2011)
10.1113/jphysiol.1965.sp007553
Water drinking in sheep with oesophageal fistulae
E. Bott (1965)
10.1002/1531-8249(199909)46:3<281::AID-ANA2>3.0.CO;2-L
The functional neuroanatomy of voluntary swallowing
D. Zald (1999)
10.1016/j.physbeh.2011.06.004
Allostasis: A model of predictive regulation
P. Sterling (2012)
10.1016/j.autneu.2008.02.001
Emetic stimulation inhibits the swallowing reflex in decerebrate rats
C. Kurozumi (2008)
10.1152/AJPREGU.1997.272.6.R1740
Regulation of fluid intake in dehydrated humans: role of oropharyngeal stimulation.
M. Figaro (1997)
10.1007/BF00236530
Identification of the medullary swallowing regions in the rat
J. Kessler (2004)
10.1073/pnas.0710572105
Effect of aging on regional cerebral blood flow responses associated with osmotic thirst and its satiation by water drinking: A PET study
M. Farrell (2008)
10.1007/s00455-002-0088-x
Activation of Cerebellum and Basal Ganglia on Volitional Swallowing Detected by Functional Magnetic Resonance Imaging
M. Suzuki (2003)
10.1016/J.NEUROIMAGE.2011.09.015
New advances in the Clinica software platform for clinical neuroimaging studies
A. Routier (2019)
10.1097/00001756-199806220-00001
Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies
T. Paus (1998)
10.1016/j.physbeh.2017.03.003
Disturbances of thirst and fluid balance associated with aging
D. Begg (2017)
10.1073/pnas.1613929113
Overdrinking, swallowing inhibition, and regional brain responses prior to swallowing
P. Saker (2016)
10.1152/AJPLEGACY.1949.159.3.533
Gastric distention as a factor in the satiation of thirst in esophagostomized dogs.
E. J. Towbin (1949)
10.1037/H0077745
Drinking in rhesus monkeys: role of presystemic and systemic factors in control of drinking.
R. Wood (1980)
10.1038/nature18950
Thirst neurons anticipate the homeostatic consequences of eating and drinking
Christopher A. Zimmerman (2016)
10.1152/JN.01144.2003
Cerebral areas processing swallowing and tongue movement are overlapping but distinct: a functional magnetic resonance imaging study.
R. Martin (2004)
10.1038/nature14108
Thirst Driving and Suppressing Signals Encoded by Distinct Neural Populations in the Brain
Yuki Oka (2015)
10.1126/SCIENCE.282.5392.1335
Role for cingulate motor area cells in voluntary movement selection based on reward.
K. Shima (1998)
10.1080/08998280.2007.11928331
Exercise-Associated Hyponatremia
W. G. Schucany (2007)
10.1038/jcbfm.1992.127
A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain
K. Worsley (1992)
10.1523/JNEUROSCI.1244-16.2016
Reciprocal Control of Drinking Behavior by Median Preoptic Neurons in Mice
S. B. Abbott (2016)
10.1016/S0960-9822(00)00584-4
Cerebellar function: Coordination, learning or timing?
M. Mauk (2000)
10.1002/hbm.20743
Neural activation of swallowing and swallowing‐related tasks in healthy young adults: An attempt to separate the components of deglutition
G. Malandraki (2009)
10.1152/AJPLEGACY.1951.166.1.142
Influence of stimulus pattern on reflex deglutition.
R. Doty (1951)



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