scholarly journals Differential neural representation of oral ethanol by central taste-sensitive neurons in ethanol-preferring and genetically heterogeneous rats

2011 ◽  
Vol 106 (6) ◽  
pp. 3145-3156 ◽  
Author(s):  
Christian H. Lemon ◽  
David M. Wilson ◽  
Susan M. Brasser

In randomly bred rats, orally applied ethanol stimulates neural substrates for appetitive sweet taste. To study associations between ethanol's oral sensory characteristics and genetically mediated ethanol preference, we made electrophysiological recordings of oral responses (spike density) by taste-sensitive nucleus tractus solitarii neurons in anesthetized selectively bred ethanol-preferring (P) rats and their genetically heterogeneous Wistar (W) control strain. Stimuli (25 total) included ethanol [3%, 5%, 10%, 15%, 25%, and 40% (vol/vol)], a sucrose series (0.01, 0.03, 0.1, 0.3, 0.5, and 1 M), and other sweet, salt, acidic, and bitter stimuli; 50 P and 39 W neurons were sampled. k-means clustering applied to the sucrose response series identified cells showing high (S1) or relatively low (S0) sensitivity to sucrose. A three-way factorial analysis revealed that activity to ethanol was influenced by a neuron's sensitivity to sucrose, ethanol concentration, and rat line ( P = 0.01). Ethanol produced concentration-dependent responses in S1 neurons that were larger than those in S0 cells. Although responses to ethanol by S1 cells did not differ between lines, neuronal firing rates to ethanol in S0 cells increased across concentration only in P rats. Correlation and multivariate analyses revealed that ethanol evoked responses in W neurons that were strongly and selectively associated with activity to sweet stimuli, whereas responses to ethanol by P neurons were not easily associated with activity to representative sweet, sodium salt, acidic, or bitter stimuli. These findings show differential central neural representation of oral ethanol between genetically heterogeneous rats and P rats genetically selected to prefer alcohol.

2014 ◽  
Vol 112 (7) ◽  
pp. 1667-1677 ◽  
Author(s):  
David M. Wilson ◽  
Christian H. Lemon

Temperature can modify neural and behavioral responses to taste stimuli that elicit “sweetness,” a perception linked to intake of calorie-laden foods. However, the role of temperature in the neural representation of sweet taste is poorly understood. Here we made electrophysiological recordings from gustatory neurons in the medulla of inbred mice to study how adjustments in taste solution temperature to cool (18°C), ambient (22°C), and warm (30°C and 37°C) values changed the magnitude and latency of gustatory activity to sucrose (0, 0.05, 0.1, 0.17, 0.31, and 0.56 M). Analysis of 22 sucrose-best neurons revealed that temperature markedly influenced responses to sucrose, which, across concentrations, were largest when solutions were warmed to 30°C. However, reducing solution temperature from warm to ambient to cool progressively steepened the slope of the sucrose concentration-response function computed across cells ( P < 0.05), indicating that mean activity to sucrose increased more rapidly with concentration steps under cooling than with warming. Thus the slope of the sucrose concentration-response function shows an inverse relation with temperature. Temperature also influenced latency to the first spike of the sucrose response. Across neurons, latencies were shorter when sucrose solutions were warmed and longer, by hundreds of milliseconds, when solutions were cooled ( P < 0.05), indicating that temperature is also a temporal parameter of sucrose activity. Our findings reveal that temperature systematically modifies the timing of gustatory activity to sucrose in the mammalian brain and how this activity changes with concentration. Results further highlight how oral somatosensory cues function as physiological modulators of gustatory processing.


2020 ◽  
Vol 45 (8) ◽  
pp. 675-685
Author(s):  
Alice Sardarian ◽  
Sophia Liu ◽  
Steven L Youngentob ◽  
John I Glendinning

Abstract Sweet flavorants enhance palatability and intake of alcohol in adolescent humans. We asked whether sweet flavorants have similar effects in adolescent rats. The inherent flavor of ethanol in adolescent rats is thought to consist of an aversive odor, bitter/sweet taste, and burning sensation. In Experiment 1, we compared ingestive responses of adolescent rats to 10% ethanol solutions with or without added flavorants using brief-access lick tests. We used 4 flavorants, which contained mixtures of saccharin and sucrose or saccharin, sucrose, and maltodextrin. The rats approached (and initiated licking from) the flavored ethanol solutions more quickly than they did unflavored ethanol, indicating that the flavorants attenuated the aversive odor of ethanol. The rats also licked at higher rates for the flavored than unflavored ethanol solutions, indicating that the flavorants increased the naso-oral acceptability of ethanol. In Experiment 2, we offered rats chow, water, and a flavored or unflavored ethanol solution every other day for 8 days. The rats consistently consumed substantially more of the flavored ethanol solutions than unflavored ethanol across the 8 days. When we switched the rats from the flavored to unflavored ethanol for 3 days, daily intake of ethanol plummeted. We conclude that sweet and sweet/maltodextrin flavorants promote high daily intake of ethanol in adolescent rats (i.e., 6–10 g/kg) and that they do so in large part by improving the naso-oral sensory attributes of ethanol.


2010 ◽  
Vol 41 (3) ◽  
pp. 232-243 ◽  
Author(s):  
Susan M. Brasser ◽  
Meghan B. Norman ◽  
Christian H. Lemon

Elevated alcohol consumption is associated with enhanced preference for sweet substances across species and may be mediated by oral alcohol-induced activation of neurobiological substrates for sweet taste. Here, we directly examined the contribution of the T1r3 receptor protein, important for sweet taste detection in mammals, to ethanol intake and preference and the neural processing of ethanol taste by measuring behavioral and central neurophysiological responses to oral alcohol in T1r3 receptor-deficient mice and their C57BL/6J background strain. T1r3 knockout and wild-type mice were tested in behavioral preference assays for long-term voluntary intake of a broad concentration range of ethanol, sucrose, and quinine. For neurophysiological experiments, separate groups of mice of each genotype were anesthetized, and taste responses to ethanol and stimuli of different taste qualities were electrophysiologically recorded from gustatory neurons in the nucleus of the solitary tract. Mice lacking the T1r3 receptor were behaviorally indifferent to alcohol (i.e., ∼50% preference values) at concentrations typically preferred by wild-type mice (5–15%). Central neural taste responses to ethanol in T1r3-deficient mice were significantly lower compared with C57BL/6J controls, a strain for which oral ethanol stimulation produced a concentration-dependent activation of sweet-responsive NTS gustatory neurons. An attenuated difference in ethanol preference between knockouts and controls at concentrations >15% indicated that other sensory and/or postingestive effects of ethanol compete with sweet taste input at high concentrations. As expected, T1r3 knockouts exhibited strongly suppressed behavioral and neural taste responses to sweeteners but did not differ from wild-type mice in responses to prototypic salt, acid, or bitter stimuli. These data implicate the T1r3 receptor in the sensory detection and transduction of ethanol taste.


2020 ◽  
Vol 150 (6) ◽  
pp. 1619-1630
Author(s):  
Carl A Roberts ◽  
Timo Giesbrecht ◽  
Nicholas Fallon ◽  
Anna Thomas ◽  
David J Mela ◽  
...  

ABSTRACT Background The reward value of palatable foods is often cited as an important influence on eating behaviors, including intake of sugars. However, human neuroimaging studies have generated conflicting evidence on the basic neural representation of taste and reward responses to caloric sweeteners (sucrose and glucose), and most relevant studies have used small subject numbers. Objective We conducted a systematic review and a coordinate-based meta-analysis of studies reporting brain responses to oral sugar solutions. Methods A systematic search of MEDLINE, Scopus, and PsycINFO through October 2019 identified fMRI studies (in healthy human adults, including those with overweight or obesity) assessing differences in responses to purified sweet and nonsweet taste stimuli. Data were extracted with the primary objective of quantifying evidence for the activation of brain regions associated with caloric sweet taste sensation. We used activation likelihood estimation meta-analysis methods. We also performed multiple sensitivity analyses to assess the generality of effects. Results Of 455 unique articles, 15 met the criteria for inclusion. These contributed to 2 primary meta-analyses: 1) sucrose (13 experiments, 179 coordinates, n = 241) and 2) sucrose + glucose (16 experiments, 209 coordinates, n = 262). Consistent activation was apparent in primary taste areas: insula (69.2% of studies) and opercular cortex (76.9% of studies), precentral gyri (53.9% of studies), and globus pallidus and postcentral gyrus (30.8% of studies for each). Evidence of reward activity (caudate) was seen in the primary analyses (30.8% of studies) but not in sensitivity analysis. Conclusions We confirm the importance of primary taste areas for gustatory processing in human adults. We also provide tentative evidence for reward-related caudate activity in relation to the sweet taste of caloric sugars. A number of factors affect the observation and interpretation of brain responses, including reward-related activity. Firm conclusions require confirmation with large data set studies.


1997 ◽  
Vol 9 (3) ◽  
pp. 607-621 ◽  
Author(s):  
Siming Lin ◽  
Jennie Si ◽  
A. B. Schwartz

The population vector method has been developed to combine the simultaneous direction-related activities of a population of motor cortical neurons to predict the trajectory of the arm movement. In this article, we consider a self-organizing model of a neural representation of the arm trajectory based on neuronal discharge rates. A self-organizing feature map (SOFM) is used to select the optimal set of weights in the model to determine the contribution of an individual neuron to an overall movement representation. The correspondence between movement directions and discharge patterns of the motor cortical neurons is established in the output map. The topology-preserving property of the SOFM is used to analyze the recorded data of a behaving monkey. The data used in this analysis were taken while the monkey was tracing spirals and doing center→out movements. The arm trajectory could be well predicted using such a statistical model based on the motor cortex neuronal firing information. The SOFM method is compared with the population vector method, which extracts information related to trajectory by assuming that each cell has a fixed preferred direction during the task. This implies that these cells are acting along lines labeled only for direction. However, extradirectional information is carried in these cell responses. The SOFM has the capability of extracting not only direction-related information but also other parameters that are consistently represented in the activity of the recorded population of cells.


1996 ◽  
Vol 19 (4) ◽  
pp. 611-631 ◽  
Author(s):  
Ralph-Axel Müller

AbstractThe concepts of the innateness, universality, species-specificity, and autonomy of the human language capacity have had an extreme impact on the psycholinguistic debate for over thirty years. These concepts are evaluated from several neurobiological perspectives, with an emphasis on the emergence of language and its decay due to brain lesion and progressive brain disease.Evidence of perceptuomotor homologies and preadaptations for human language in nonhuman primates suggests a gradual emergence of language during hominid evolution. Regarding ontogeny, the innate component of language capacity is likely to be polygenic and shared with other developmental domains. Dissociations between verbal and nonverbal development are probably rooted in the perceptuomotor specializations of neural substrates rather than the autonomy of a grammar module. Aphasiologicaldata often assumed to suggest modular linguistic subsystems can be accounted for in terms of a neurofunctional model incorporating perceptuomotor-based regional specializationsand distributivity of representations. Thus, dissociations between grammatical functors and content words are due to different conditions of acquisition and resulting differences in neural representation. Human brains are characterized by multifactorial interindividual variability, and strict universality of functional organization is biologically unrealistic.A theoretical alternative is proposed according to which (1) linguistic specialization of brain areas is due to epigenetic and probabilistic maturational events, not to genetic ”hard-wiring,” and (2) linguistic knowledge is neurally represented in distributed cell assemblies whose topography reflects the perceptuomotor modalities involved in the acquisition and use of a given item of knowledge.


2012 ◽  
Vol 108 (5) ◽  
pp. 1288-1298 ◽  
Author(s):  
Cheng-Shu Li ◽  
Sooyoung Chung ◽  
Da-Peng Lu ◽  
Young K. Cho

The parabrachial nuclei (PbN), the second central relay for the gustatory pathway, transfers taste information to various forebrain gustatory nuclei and to the gustatory cortex. The nucleus accumbens is one of the critical neural substrates of the reward system, and the nucleus accumbens shell region (NAcSh) is associated with feeding behavior. Taste-evoked neuronal responses of PbN neurons are modulated by descending projections from the gustatory nuclei in the forebrain. In the present study, we investigated whether taste-responsive neurons in the PbN project to the NAcSh and whether pontine gustatory neurons are subject to modulatory influence from the NAcSh in urethane-anesthetized hamsters. Extracellular single-unit activity was recorded in the PbN, and taste responses were confirmed by the delivery of 32 mM sucrose, NaCl, quinine hydrochloride, and 3.2 mM citric acid to the anterior tongue. The NAcSh was then stimulated (0.5 ms, ≤100 μA) bilaterally using concentric bipolar stimulating electrodes. A total of 98 taste neurons were recorded from the PbN. Eighteen neurons were antidromically invaded from the NAcSh, mostly the ipsilateral NAcSh ( n = 16). Stimulation of the ipsilateral and contralateral NAcSh suppressed the neuronal activity of 88 and 55 neurons, respectively; 52 cells were affected bilaterally. In a subset of pontine neurons tested, electrical stimulation of the NAcSh during taste stimulation also suppressed taste-evoked neuronal firing. These results demonstrated that taste-responsive neurons in the PbN not only project to the NAcSh but also are under substantial descending inhibitory influence from the bilateral NAcSh.


2019 ◽  
Author(s):  
Aniruddha Das ◽  
Chinthasagar Bastian ◽  
Lexie Trestan ◽  
Jason Suh ◽  
Tanujit Dey ◽  
...  

AbstractDemyelination of axons in the central nervous system (CNS) is a hallmark of multiple sclerosis (MS) and other demyelinating diseases. Cycles of demyelination, followed by remyelination, appear in the majority of MS patients, and are associated with the onset and quiescence of disease-related symptoms, respectively. Previous studies have shown in human patients and animal models that vast demyelination is accompanied by wide-scale changes to brain activity, but details of this process are poorly understood. We use electrophysiological recordings and nonlinear imaging of fluorescence from genetically-encoded calcium indicators to monitor the activity of hippocampal neurons during demyelination and remyelination processes over a period of 100 days. We find in vitro that synaptic transmission in CA1 neurons is diminished, and in vivo both CA1 and dentate gyrus (DG) neuronal firing rates are substantially reduced during demyelination and partially recover after a short remyelination period. This new approach allows monitoring how synaptic transmission changes, induced by cuprizone diet, are affecting neuronal activity, and can potentially be used to study the effects of therapeutic interventions in protecting the functionality of CNS neurons.


2010 ◽  
Vol 104 (4) ◽  
pp. 2224-2235
Author(s):  
Ida Siveke ◽  
Christian Leibold ◽  
Katharina Kaiser ◽  
Benedikt Grothe ◽  
Lutz Wiegrebe

The mammalian binaural system compares the timing of monaural inputs with microsecond precision. This temporal precision is required for localizing sounds in azimuth. However, temporal features of the monaural inputs, in particular their latencies, highly depend on the overall sound level. In a combined psychophysical, electrophysiological, and modeling approach, we investigate how level-dependent latency shifts of the monaural responses are reflected in the perception and neural representation of interaural time differences. We exploit the sensitivity of the binaural system to the timing of high-frequency stimuli with binaurally incongruent envelopes. Using these novel stimuli, both the perceptually adjusted interaural time differences and the time differences extracted from electrophysiological recordings systematically depend on overall sound pressure level. The perceptual and electrophysiological time differences of the envelopes can be explained in an existing model of temporal integration only if a level-dependent firing threshold is added. Such an adjustment of firing threshold provides a temporally accurate neural code of the temporal structure of a stimulus and its binaural disparities independent of overall sound level.


2019 ◽  
Vol 14 (8) ◽  
pp. 815-826 ◽  
Author(s):  
Zhenhong He ◽  
Dandan Zhang ◽  
Nils Muhlert ◽  
Rebecca Elliott

Abstract Depression has been reliably associated with abnormalities in the neural representation of reward and loss. However, most studies have focused on monetary incentives; fewer studies have considered neural representation of social incentives. A direct comparison of non-social and social incentives within the same study would establish whether responses to the different incentives are differentially affected in depression. The functional magnetic resonance imaging study presented here investigated the neural activity of individuals with subthreshold depression (SD) and healthy controls (HCs) while they participated in an incentive delay task offering two types of reward (monetary gain vs social approval) and loss (monetary loss vs social disapproval). Compared to HCs, individuals with SD showed increased subgenual anterior cingulate cortex (sgACC) activity during anticipation of social loss, whereas the response in the putamen was decreased during consumption of social gain. Individuals with SD also exhibited diminished insula responses in consuming social loss. Furthermore, positive connectivity between the insula and ventral lateral pre-frontal cortex (VLPFC) was observed in individuals with SD while negative connectivity was found in HCs when consuming social loss. These results demonstrate neural alterations in individuals with depression, specific to the processing of social incentives, mainly characterised by dysfunction within the ‘social pain network’ (sgACC, insula and VLPFC).


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