Effects of Cue-Triggered Expectation on Cortical Processing of Taste

Department of Neurobiology and Behavior, State University of New York at Stony Brook, Stony Brook, NY 11794, USA.
Neuron (Impact Factor: 15.98). 04/2012; 74(2):410-22. DOI: 10.1016/j.neuron.2012.02.031
Source: PubMed

ABSTRACT Animals are not passive spectators of the sensory world in which they live. In natural conditions they often sense objects on the bases of expectations initiated by predictive cues. Expectation profoundly modulates neural activity by altering the background state of cortical networks and modulating sensory processing. The link between these two effects is not known. Here, we studied how cue-triggered expectation of stimulus availability influences processing of sensory stimuli in the gustatory cortex (GC). We found that expected tastants were coded more rapidly than unexpected stimuli. The faster onset of sensory coding related to anticipatory priming of GC by associative auditory cues. Simultaneous recordings and pharmacological manipulations of GC and basolateral amygdala revealed the role of top-down inputs in mediating the effects of anticipatory cues. Altogether, these data provide a model for how cue-triggered expectation changes the state of sensory cortices to achieve rapid processing of natural stimuli.

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Available from: Chad Samuelsen, Mar 26, 2015
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    • "The role of sensory areas—especially primary sensory areas—has long been regarded as providing a faithful representation of the external world (Felleman and Van Essen, 1991; Goldman-Rakic , 1988; Kandel et al., 2000; Miller and Cohen, 2001); several studies have shown that these areas convey sensory information (Ghazanfar and Schroeder, 2006; Hubel and Wiesel, 1962, 1968; Lemus et al., 2010; Liang et al., 2013), while others have shown causal roles in sensory perception (Glickfeld et al., 2013; Jaramillo and Zador, 2011; Sachidhanandam et al., 2013; Znamenskiy and Zador, 2013). However, this view has recently been challenged by observations that sensory cortices represent not only stimulus features, but also non-sensory information (Abolafia et al., 2011; Ayaz et al., 2013; Brosch et al., 2011; Fontanini and Katz, 2008; Gavornik and Bear, 2014; Jaramillo and Zador, 2011; Keller et al., 2012; Niell and Stryker, 2010; Niwa et al., 2012; Pantoja et al., 2007; Samuelsen et al., 2012; Serences, 2008; Shuler and Bear, 2006; St anis xor et al., 2013; Zelano et al., 2011). In the visual modality, it has been shown that V1 can predict the learned typical interval between a stimulus and a reward (Chubykin et al., 2013; Shuler and Bear, 2006), and that the ability to learn such intervals depends on cholinergic input from the basal forebrain (Chubykin et al., 2013). "
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    ABSTRACT: Most behaviors are generated in three steps: sensing the external world, processing that information to instruct decision-making, and producing a motor action. Sensory areas, especially primary sensory cortices, have long been held to be involved only in the first step of this sequence. Here, we develop a visually cued interval timing task that requires rats to decide when to perform an action following a brief visual stimulus. Using single-unit recordings and optogenetics in this task, we show that activity generated by the primary visual cortex (V1) embodies the target interval and may instruct the decision to time the action on a trial-by-trial basis. A spiking neuronal model of local recurrent connections in V1 produces neural responses that predict and drive the timing of future actions, rationalizing our observations. Our data demonstrate that the primary visual cortex may contribute to the instruction of visually cued timed actions. Copyright © 2015 Elsevier Inc. All rights reserved.
    Neuron 03/2015; DOI:10.1016/j.neuron.2015.02.043 · 15.98 Impact Factor
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    • "This is not to say that the dynamics observed in the present study are completely independent of mode of stimulus presentation. Indeed, behavioral context has previously shown to influence taste responses and dynamics of taste coding profoundly (Fontanini and Katz 2006; Samuelsen et al. 2012; Stapleton et al. 2006; Yoshida and Katz 2011). We do not yet know how mixture coding early in the response to taste mixtures may change with behavioral context. "
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    ABSTRACT: Taste stimuli encountered in the natural environment are usually combinations of multiple tastants. Although a great deal is known about how neurons in the taste system respond to single taste stimuli in isolation, less is known about how the brain deals with such mixture stimuli. Here, we probe the responses of single neurons in primary gustatory cortex (GC) of awake rats to an array of taste stimuli including 100% citric acid (100 mM), 100% sodium chloride (100 mM) 100% sucrose (100 mM), and a range of binary mixtures (90%/10%, 70%/30%, 50%/50%, 30%/70% and 10%/90%). We tested for the presence of three different hypothetical response patterns: 1) responses varying monotonically as a function of concentration of sucrose (or acid) in the mixture (the "monotonic" pattern); 2) responses increasing or decreasing as a function of degree of mixture of the stimulus (the "mixture" pattern); and 3) responses that change abruptly from being similar to one pure taste to being similar the other (the "categorical" pattern). Our results demonstrate the presence of both monotonic and mixture patterns within responses of GC neurons. Specifically, further analysis (that included the presentation of 50 mM sucrose and citric acid) made it clear that mixture suppression reliably precedes a palatability-related pattern. The temporal dynamics of the emergence of the palatability-related pattern parallel the temporal dynamics of the emergence of preference behavior for the same mixtures, as measured by a brief access test. We saw no evidence of categorical coding.
    Journal of Neurophysiology 01/2013; 109(8). DOI:10.1152/jn.00917.2012 · 3.04 Impact Factor
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    • "Although the orientation of the rat's head while obtaining water as a cue or reward may explain some of these differences (the rewarded choice lick spouts were positioned on either side of the rat), this explanation seems unlikely for all cases because nearly a third of the water selective neurons showed a strong excitatory response to water as a cue but no response at all to water when presented as a reward (Figure 4C). Rather, these results lend support to the idea that tastant processing in the GC may be influenced by the behavioural context that underlies the taste (Yoshida & Katz, 2011; Samuelsen et al. 2012). "
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    ABSTRACT: The gustatory cortex (GC) is important for perceiving the intensity of tastants but it remains unclear as to how single neurons in the region carry out this function. Previous studies have shown that taste-evoked activity from single neurons in GC can be correlated or anticorrelated with tastant concentration, yet whether one or both neural responses signal intensity is poorly characterized because animals from these studies were not trained to report the intensity of the concentration that they tasted. To address this issue, we designed a two-alternative forced choice (2-AFC) task in which freely licking rats distinguished among concentrations of NaCl and recorded from ensembles of neurons in the GC. We identified three neural ensembles that rapidly (<300 ms or ∼2 licks) processed NaCl concentration. For two ensembles, their NaCl evoked activity was anticorrelated with NaCl concentration but could be further distinguished by their response to water; in one ensemble, water evoked the greatest response while in the other ensemble the lowest tested NaCl concentration evoked the greatest response. However, the concentration sensitive activity from each of these ensembles did not show a strong association with the behaviour of the rat in the 2-AFC task, suggesting a lesser role for signalling tastant intensity. Conversely, for a third neural ensemble, its neural activity was well correlated with increases in NaCl concentration, and this relationship best matched the intensity perceived by the rat. These results suggest that this neuronal ensemble in GC whose activity monotonically increases with concentration plays an important role in signalling the intensity of the taste of NaCl.
    The Journal of Physiology 05/2012; 590(Pt 13):3169-84. DOI:10.1113/jphysiol.2012.233486 · 4.54 Impact Factor
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