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Research Articles, Systems/Circuits

A Novel Mechanism for T1R-Independent Taste Responses to Concentrated Sugars

B. Kalyanasundar, Ginger D. Blonde, Alan C. Spector and Susan P. Travers
Journal of Neuroscience 8 February 2023, 43 (6) 965-978; DOI: https://doi.org/10.1523/JNEUROSCI.1760-22.2023
B. Kalyanasundar
1Division of Biosciences, College of Dentistry, Ohio State University, Columbus, Ohio, 43210-1267
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Ginger D. Blonde
2Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, Florida, 32306-4301
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Alan C. Spector
2Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, Florida, 32306-4301
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Susan P. Travers
1Division of Biosciences, College of Dentistry, Ohio State University, Columbus, Ohio, 43210-1267
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Abstract

Recent findings from our laboratory demonstrated that the rostral nucleus of the solitary tract (rNST) retains some responsiveness to sugars in double-knock-out mice lacking either the T1R1+T1R3 (KO1+3) or T1R2+T1R3 (KO2+3) taste receptor heterodimers. Here, we extended these findings in the parabrachial nucleus (PBN) of male and female KO1+3 mice using warm stimuli to optimize sugar responses and employing additional concentrations and pharmacological agents to probe mechanisms. PBN T1R-independent sugar responses, including those to concentrated glucose, were more evident than in rNST. Similar to the NST, there were no “sugar-best” neurons in KO1+3 mice. Nevertheless, 1000 mm glucose activated nearly 55% of PBN neurons, with responses usually occurring in neurons that also displayed acid and amiloride-insensitive NaCl responses. In wild-type (WT) mice, concentrated sugars activated the same electrolyte-sensitive neurons but also “sugar-best” cells. Regardless of genotype, phlorizin, an inhibitor of the sodium-glucose co-transporter (SGLT), a component of a hypothesized alternate glucose-sensing mechanism, did not diminish responses to 1000 mm glucose. The efficacy of concentrated sugars for driving neurons broadly responsive to electrolytes implied an origin from Type III taste bud cells. To test this, we used the carbonic anhydrase (CA) inhibitor dorzolamide (DRZ), previously shown to inhibit amiloride-insensitive sodium responses arising from Type III taste bud cells. Dorzolamide had no effect on sugar-elicited responses in WT sugar-best PBN neurons but strongly suppressed them in WT and KO1+3 electrolyte-generalist neurons. These findings suggest a novel T1R-independent mechanism for hyperosmotic sugars, involving a CA-dependent mechanism in Type III taste bud cells.

SIGNIFICANCE STATEMENT Since the discovery of Tas1r receptors for sugars and artificial sweeteners, evidence has accrued that mice lacking these receptors maintain some behavioral, physiological, and neural responsiveness to sugars. But the substrate(s) has remained elusive. Here, we recorded from parabrachial nucleus (PBN) taste neurons and identified T1R-independent responses to hyperosmotic sugars dependent on carbonic anhydrase (CA) and occurring primarily in neurons broadly responsive to NaCl and acid, implying an origin from Type III taste bud cells. The effectiveness of different sugars in driving these T1R-independent responses did not correlate with their efficacy in driving licking, suggesting they evoke a nonsweet sensation. Nevertheless, these salient responses are likely to comprise an adequate cue for learned preferences that occur in the absence of T1R receptors.

  • broadly-tuned taste neurons
  • hyperosmotic sugars
  • parabrachial nucleus
  • Type 1 taste receptors
  • Type III taste bud cells

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The Journal of Neuroscience: 43 (6)
Journal of Neuroscience
Vol. 43, Issue 6
8 Feb 2023
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A Novel Mechanism for T1R-Independent Taste Responses to Concentrated Sugars
B. Kalyanasundar, Ginger D. Blonde, Alan C. Spector, Susan P. Travers
Journal of Neuroscience 8 February 2023, 43 (6) 965-978; DOI: 10.1523/JNEUROSCI.1760-22.2023

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A Novel Mechanism for T1R-Independent Taste Responses to Concentrated Sugars
B. Kalyanasundar, Ginger D. Blonde, Alan C. Spector, Susan P. Travers
Journal of Neuroscience 8 February 2023, 43 (6) 965-978; DOI: 10.1523/JNEUROSCI.1760-22.2023
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Keywords

  • broadly-tuned taste neurons
  • hyperosmotic sugars
  • parabrachial nucleus
  • Type 1 taste receptors
  • Type III taste bud cells

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