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Breza-Leptin-Increases.Pdf Physiology & Behavior 107 (2012) 533–539 Contents lists available at SciVerse ScienceDirect Physiology & Behavior journal homepage: www.elsevier.com/locate/phb Leptin increases temperature-dependent chorda tympani nerve responses to sucrose in mice Bo Lu a,b, Joseph M. Breza b, Alexandre A. Nikonov b, Andrew B. Paedae b, Robert J. Contreras b,⁎ a Department of Physiology and Pathophysiology, Xi'an Jiaotong University School of Medicine, 76# W. Yanta Road, Xi'an, Shaanxi, 710061, PR China b Department of Psychology and Program in Neuroscience, Florida State University, Tallahassee, FL 32306-4301, USA article info abstract Article history: Leptin receptors are present in taste buds and previous research indicates that leptin administration modified Received 15 December 2011 electrophysiological and behavioral responses to sweet taste. It is now known that sweet taste is temperature Received in revised form 17 April 2012 dependent. We examined the influence of (1) stimulus temperature on chorda tympani (CT) nerve re- Accepted 19 April 2012 sponses to sucrose, saccharin and NH4Cl; and (2) leptin administration on CT nerve responses to sucrose, saccharin and other basic taste stimuli at 35 °C that maximized sweet-taste sensitivity in C57BL/6 mice. Keywords: We found that the CT nerve responded with greater magnitude to sucrose and saccharin as stimulus Temperature Sweet taste temperature increased from 23 to 35 °C and then declined at higher temperatures. In contrast, the CT Leptin nerve responses to NH4Cl increased in magnitude as temperature increased from 23 to 44 °C. We also Chorda tympani nerve showed that leptin selectively increased the CT nerve responses to sucrose at 35 °C in both fasted Mice and free-fed mice. The responses of mice treated with the saline vehicle did not change. Our findings are consistent with the notion that leptin binds with its receptors in fungiform taste buds and alters the message conveyed by sugar-responsive neurons to the brain. © 2012 Elsevier Inc. All rights reserved. 1. Introduction responsive to a broad range of sugars and artificial sweeteners [6,7]. There is also a T1R-independent mechanism for sweet-taste trans- The adipose-derived hormone leptin is well known for the key duction involving glucose transporters [8,9]. Many studies, including role it plays in suppressing consumption and increasing energy expen- our own, have shown that sweet taste sensitivity is temperature diture by its action on leptin receptors in critical hypothalamic nuclei dependent [10,11]. It has been shown that a member of the tran- [1,2]. Less well studied is the role of leptin in altering taste function. sient receptor potential (TRP) superfamily of ion channels, TRPM5, Kawai, et al. [3] were the first to study the influence of leptin on taste. underlies the temperature-dependent nature of sweet taste [12–14]. They showed that intraperitoneal administration of leptin into fasted TRPM5 is a Ca2+- and voltage-activated nonselective cation channel mice reduced the integrated responses of the chorda tympani (CT) that is a working component downstream from the G-protein- and glossopharyngeal (GL) nerves to ≈24 °C sucrose and saccharin, coupled sweet taste receptor, T1R2 and T1R3 [6,15–18], and is thought but not to NaCl, HCl, or QHCl. They showed further in patch-clamp to amplify the taste signal by facilitating taste cell depolarization. In studies of isolated taste receptors cells from circumvallate papillae fact, TRPM5 knockout (KO) mice have greatly reduced, but not that leptin activated outward potassium currents and hyperpolarized abolished responses of the CT nerve to sweet compounds, suggesting taste cells making them less responsive to taste stimulation [3].These the existence of TRPM5-dependent and TRPM5-independent trans- electrophysiological findings were followed by anatomical evidence duction pathways for sweet taste [7,19]. In addition, TRPM5 is a demonstrating that leptin receptors were located on taste buds of heat-activated channel whose activity has been shown to increase be- fungiform and circumvallate papillae [4,5]. This story is, however, incom- tween 15° and 35 °C [14,20]. plete because it is not yet known whether leptin receptors, activated To date, the only electrophysiological study that has investigated potassium currents and hyperpolarization occur only in taste cells the influence of leptin on taste nerve responses was done using with the machinery for sweet taste transduction. chemical stimuli delivered at room temperature (≈24 °C) to the Sweet-taste transduction involves two G protein-coupled recep- lingual taste buds [3]. This study was performed under less than tors, T1R2 and T1R3, which dimerize to form the sweet receptor optimal conditions before the influential role of temperature and TRPM5 on sweet taste was thoroughly appreciated. We have had a long-standing interest in how temperature influences neural res- ⁎ Corresponding author at: Department of Psychology and Program in Neuroscience, ponses to chemical stimulation of lingual receptors [10,21–23].Because Florida State University, 1107 West Call St., Tallahassee, Florida, 32306-4301, USA. Tel.: +1 8506441083; fax: +1 8506449656. of this interest, we have adopted a stimulus delivery system with which E-mail address: [email protected] (R.J. Contreras). we can control the temperature of the stimulus solutions over a wide 0031-9384/$ – see front matter © 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.physbeh.2012.04.018 534 B. Lu et al. / Physiology & Behavior 107 (2012) 533–539 temperature range. Accordingly, we conducted the present study to preceding each chemical stimulus presentation was subtracted from serve two main purposes. Our first purpose was to confirm and extend the integrated response resulting from the 10-s stimulus to calculate prior work investigating the influence of temperature on sweet taste the area under the curve (AUC). using our stimulus delivery system in mice. We examined the influence of stimulating temperature on the CT nerve responses to sucrose, sac- 3. Experiment 1 charin, and NH4Cl from 23 to 44 °C in C57BL/6 mice. Our second purpose fl was to extend prior work investigating the in uence of leptin adminis- In this experiment, we tested the influence of temperature on CT tration on the CT nerve responses to sucrose, saccharin and other basic nerve responses to a sucrose concentration series and to a single con- taste stimuli at 35 °C that maximized sweet-taste sensitivity. centration of sodium saccharin and NH4Cl. 2. Materials and general methods 3.1. Subjects and taste protocol 2.1. Subjects Six mice were used to investigate the effects of different tempera- tures on CT nerve responses to sweet stimuli. For each mouse, we Adult male C57BL/J6 (Jackson Laboratory, Bar Harbor, ME) mice recorded CT nerve responses to a sucrose concentration series (0.1, weighing 26–32 g at the start of the experiments were housed indi- 0.3, 0.6 and 1.0 M sucrose) and to 0.02 M sodium saccharin and vidually in transparent plastic cages in a temperature-controlled col- 0.1 M NH Cl at eight different temperatures in 3 °C intervals from ony room (22 °C–24 °C) and maintained on a 12:12-h light–dark 4 23 to 44 °C. To control for individual differences among preparations, cycle with lights on at 7:00 am. All the animals were habituated to we also applied 0.6 M NaCl periodically during the recording session. the animal facility for at least 1 week before CT recording or behavior- The AUC responses to the sweet stimuli and NH Cl were normalized al testing. All mice had ad libitum access to Purina Rat Chow (no. 4 to the average response to 0.6 M NaCl for each animal. We used 5001) and de-ionized water unless otherwise indicated. The Institu- 0.6 M NaCl for normalization in this experiment because our prelim- tional Animal Care and Use Committee at Florida State University ap- inary tests indicated that CT nerve responses to NaCl stimuli were proved all procedures. least affected by differences in stimulus temperature. The response to 0.6 M NaCl was also used to evaluate the stability of the prepara- 2.2. Electrophysiological recordings of taste responses of the mouse tion. A recording was considered stable when the responses to chorda tympani 0.6 M NaCl at the beginning and at the end of each stimulation series deviated by no more than 15%. Only responses from stable recordings The mice were anesthetized with intraperitoneal administration were used for data analysis. of ketamine (30 mg/kg body weight) followed by urethane (1.2 g/kg). Supplemental urethane injections were given to maintain a deep level of anesthesia without reflex response to foot pinch. The mice 3.2. Data analysis were tracheotomized with PE50 tubing, and secured in a non- traumatic head holder (Model 926B Mouse Nose/Tooth Bar Assembly, All data are presented as group means±SEM. Differences be- David Kopf Instruments, Tujunga, CA). Using a mandibular approach, tween the responses at different temperatures were performed the right CT branch of the facial nerve was exposed and transected using two-way and one-way repeated measure ANOVA followed by fi where it enters the tympanic bulla. The CT nerve was desheathed, post hoc pairwise comparisons using contrast coef cients. All analy- and placed on a platinum wire electrode (positive polarity) and the ses were performed using Statistical Program for Social Sciences soft- fi b entire cavity was then filled with high quality paraffin oil (VWR) to ware (SPSS 13.0) with statistical signi cance accepted when P 0.05. isolate the nerve signal from ground and maintain nerve integrity. An indifferent electrode (negative polarity) was attached to the skin 3.3. Results overlying the cranium with a tinned-copper alligator clip. Neural activ- ity was differentially amplified (X10,000; A-M Systems, Sequim, WA, A two-way repeated measures ANOVA showed that the CT nerve bandpass 300–5000 Hz), observed with an oscilloscope, digitized with responses to sucrose varied significantly as a function of stimulus waveform hardware and software (Spike 2; Cambridge Electronic concentration [F(1.25,189.75)=136.90, Pb0.001] and stimulus tem- Design, Cambridge, England), and stored on a computer for off-line perature [F(1.61,189.39)=4.67, Pb0.01].
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