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: 15.05). 04/2012; 74(2):410-22. DOI: 10.1016/j.neuron.2012.02.031
Source: PubMed


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; 86(1). DOI:10.1016/j.neuron.2015.02.043 · 15.05 Impact Factor
    • "These inputs are distinct in terms of the cortical areas they target and their function. Projections directly from limbic structures tend to be more diffuse within the insular cortex (Allen et al., 1991), and are implicated in affective aspects of gustatory processing (Piette et al., 2012; Samuelsen et al., 2012). In contrast, thalamocortical projections from the VPMpc largely terminate in the granular and dysgranular insular cortex, and provide orosensory aspects of taste processing (Sewards, 2004; Samuelsen et al., 2013). "
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    ABSTRACT: Ventroposterior medialis parvocellularis (VPMpc) of thalamus, the thalamic relay nucleus for gustatory sensation, receives primary input from parabrachial nucleus, and projects to insular cortex. To reveal unique properties of gustatory thalamus in comparison to archetypical sensory relay nuclei, this study examines the morphology of synaptic circuitry in VPMpc, focusing on parabrachiothalamic driver input and corticothalamic feedback. Anterogradely visualized parabrachiothalamic fibers in VPMpc bear large swellings. At electron microscope resolution, parabrachiothalamic axons are myelinated and make large boutons, forming multiple asymmetric, adherent and perforated synapses onto large caliber dendrites and dendrite initial segments. Labeled boutons contain dense-core vesicles, and they resemble a population of calcitonin gene-related peptide containing terminals within VPMpc. As typical of primary inputs to other thalamic nuclei, parabrachiothalamic terminals are over 5 times larger than other inputs, while constituting only 2% of all synapses. Glomeruli and triadic arrangements, characteristic features of other sensory thalamic nuclei, are not encountered. As revealed by anterograde tracer injections into insular cortex, corticothalamic projections in VPMpc form a dense network of fine fibers bearing small boutons. Corticothalamic terminals within VPMpc were also observed to synapse on cells that were retrogradely filled from the same injections. The results constitute an initial survey in describing unique anatomical properties of rodent gustatory thalamus. J. Comp. Neurol., 2014. © 2014 Wiley Periodicals, Inc.
    The Journal of Comparative Neurology 01/2015; 523(1). DOI:10.1002/cne.23673 · 3.23 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 · 2.89 Impact Factor
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