Intragastric drinking in the rat: Evidence for a role of oropharyngeal stimulation

Altar, Anthony; Carlisle, Harry J.

doi:10.1016/0031-9384(79)90281-6

Cited by 48 publications

(5 citation statements)

References 18 publications

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“…We considered the possibility that the activation of dopamine neurons by systemic rehydration could be involved in this learning process. Of note, although water rewards are widely used to train animals 50 , attempts to bypass normal drinking and drive operant behaviour with intragastric fluids alone have been unsuccessful 51,52 . However, we reasoned that changes in fluid balance might be more efficient at driving learning about oral cues such as flavours, since these two modalities are tightly coupled during normal ingestion.…”

Section: Role Of Dopamine In Learning About Fluidsmentioning

confidence: 99%

Dopamine subsystems that track internal states

Grove

Gray

Medina

et al. 2022

Nature

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Food and water are rewarding in part because they satisfy our internal needs1,2. Dopaminergic neurons in the ventral tegmental area (VTA) are activated by gustatory rewards3–5, but how animals learn to associate these oral cues with the delayed physiological effects of ingestion is unknown. Here we show that individual dopaminergic neurons in the VTA respond to detection of nutrients or water at specific stages of ingestion. A major subset of dopaminergic neurons tracks changes in systemic hydration that occur tens of minutes after thirsty mice drink water, whereas different dopaminergic neurons respond to nutrients in the gastrointestinal tract. We show that information about fluid balance is transmitted to the VTA by a hypothalamic pathway and then re-routed to downstream circuits that track the oral, gastrointestinal and post-absorptive stages of ingestion. To investigate the function of these signals, we used a paradigm in which a fluid’s oral and post-absorptive effects can be independently manipulated and temporally separated. We show that mice rapidly learn to prefer one fluid over another based solely on its rehydrating ability and that this post-ingestive learning is prevented if dopaminergic neurons in the VTA are selectively silenced after consumption. These findings reveal that the midbrain dopamine system contains subsystems that track different modalities and stages of ingestion, on timescales from seconds to tens of minutes, and that this information is used to drive learning about the consequences of ingestion.

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Section: Role Of Dopamine In Learning About Fluidsmentioning

confidence: 99%

Dopamine subsystems that track internal states

Grove

Gray

Medina

et al. 2022

Nature

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“…provide only indirect evidence on the role of orosensory inputs, by manipulating diet palatability (e.g., Le Magnen, 1971;Peck, 1978), bypassing orosensory receptors (e.g., Altar & Carlisle, 1979;Snowdon, 1969), or disrupting orogastric contingencies (e.g., Blass & Hall, 1976;Davis & Levine, 1977). With the exception of a few early studies (Bellows & van Wagenen, 1939;Pfaffmann, 1952;Richter, 1956), little use has been made of the deafferentation experiment, the traditional physiological procedure for assessing the contribution of afferent mechanisms to the control of specific behaviors.…”

mentioning

confidence: 99%

Trigeminal orosensation and ingestive behavior in the rat.

Zeiguer¹,

Jacquin²,

Miller³

1983

Behavioral Neuroscience

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A deafferentation procedure was used to examine the contributions of trigeminal orosensation to the control of ingestive behavior in the rat. The procedure removed somatosensory input from the mouth, sparing olfaction, lingual taste, and vibrissae inputs as well as proprioceptive afferents from and efferents to the jaw muscles. Rats with sections of tongue or jaw muscle efferents served as oromotor controls. Bilateral trigeminal orosensory deafferentation was followed by an array of effects on ingestive behavior whose magnitudes were proportional to the extent of the deafferentation. The "trigeminal syndrome" includes a disruption of food and water intake (aphagia, adipsia), impairments in the sensorimotor control of eating and drinking, decreased responsiveness to food and water, and a reduction in the level of body weight regulation. Trigeminal deafferentation spared elementary ingestive movement patterns (biting, licking, chewing) but disrupted their control by the perioral stimuli, which normally elicit them, so that eating and drinking sequences were either aborted or inefficient. Deficits in food intake varied with the sensory properties of the diet. Recovery of intake took place along a palatability gradient, and recovery of water intake paralleled that of dry food. The chronically reduced body weight was caused by a persistent hypophagia and reflects reduced responsiveness to food. These findings suggest a considerable degree of overlap in the neural mechanisms mediating the sensorimotor and motivational control of intake in the rat.

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“…Although oral sensory inputs have been reported to be a contributing factor in the control of food and water intake (Altar & Carlisle, 1979;Epstein, 1967;Holman, 1968;Marshall & Teitelbaum, 1974;Nicolaidis & Rowland, 1977;Snowdon, 1969), their precise role has remained unclear. Only in pigeons has it been demonstrated that selective elimination of one sensory system, intraoral trigeminal somatosensation, leads to aphagia and hypophagia due to insufficient initiation of feeding bouts (Miller, Zeigler, & Miller, 1978;Zeigler, 1973).…”

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confidence: 99%

Trigeminal deafferentation and ingestive behavior in rats.

Miller¹

1981

Journal of Comparative and Physiological Psychology

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For studying the role of orosensory input in the control of ingestive behavior, rats were subjected to varying degrees of trigeminal deafferentation. Somatosensory branches that convey touch, temperature, and pain from the oral cavity were sectioned selectively, and innervation of the muscles of mastication and taste afferents were left intact. Severe intake deficits were produced, which included aphagia, adipsia, and prolonged hypophagia accompanied by a corresponding decrease in body weight. The deficits were proportional to the extent of deafferentation and were most severe when upper and lower portions of the mouth were affected. Although somatosensory impairment affected the organization of the consummatory response, all rats could bite, chew, and lick. Analysis of feeding patterns of minimally (mandibular) deafferented rats showed that the animals compensated for the consummatory inefficiency by increasing meal duration but failed to initiate meals at the normal rate, thus keeping food intake below normal levels. These results suggest that oral somatosensory input is critical for the mechanisms that regulate ingestive behavior.

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Intragastric drinking in the rat: Evidence for a role of oropharyngeal stimulation

Cited by 48 publications

References 18 publications

Dopamine subsystems that track internal states

Dopamine subsystems that track internal states

Trigeminal orosensation and ingestive behavior in the rat.

Trigeminal deafferentation and ingestive behavior in rats.

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