Odor- and state-dependent olfactory tubercle local field potential dynamics in awake rats

Carlson, Kaitlin S.; Dillione, Maggie R.; Wesson, Daniel W.

doi:10.1152/jn.00829.2013

Cited by 23 publications

(23 citation statements)

References 88 publications

(125 reference statements)

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“…This indirect mechanism could be by shaping motivation and/or the reward features of the odors (e.g., via modulation of structures identified in Figure 4). Directly, OT stimulation might perturb basic aspects of odor processing known to occur in the OT (Wesson and Wilson, 2010; Payton et al, 2012; Carlson et al, 2014) and thus alter odor perception more specifically. We predict that the effects observed in the present paper stem form a combination of both direct and indirect impacts of OT activity on behavior.…”

Section: Discussionmentioning

confidence: 99%

Olfactory tubercle stimulation alters odor preference behavior and recruits forebrain reward and motivational centers

FitzGerald

Richardson

Wesson

2014

Front. Behav. Neurosci.

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Rodents show robust behavioral responses to odors, including strong preferences or aversions for certain odors. The neural mechanisms underlying the effects of odors on these behaviors in animals are not well understood. Here, we provide an initial proof-of-concept study into the role of the olfactory tubercle (OT), a structure with known anatomical connectivity with both brain reward and olfactory structures, in regulating odor-motivated behaviors. We implanted c57bl/6 male mice with an ipsilateral bipolar electrode into the OT to administer electric current and thereby yield gross activation of the OT. We confirmed that electrical stimulation of the OT was rewarding, with mice frequently self-administering stimulation on a fixed ratio schedule. In a separate experiment, mice were presented with either fox urine or peanut odors in a three-chamber preference test. In absence of OT stimulation, significant preference for the peanut odor chamber was observed which was abolished in the presence of OT stimulation. Perhaps providing a foundation for this modulation in behavior, we found that OT stimulation significantly increased the number of c-Fos positive neurons in not only the OT, but also in forebrain structures essential to motivated behaviors, including the nucleus accumbens and lateral septum. The present results support the notion that the OT is integral to the display of motivated behavior and possesses the capacity to modulate odor hedonics either by directly altering odor processing or perhaps by indirect actions on brain reward and motivation structures.

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Section: Discussionmentioning

confidence: 99%

Olfactory tubercle stimulation alters odor preference behavior and recruits forebrain reward and motivational centers

FitzGerald

Richardson

Wesson

2014

Front. Behav. Neurosci.

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“…Only 4 were later utilized for electrophysiology data analyses due to electrode placement errors, poor signals, or inability to perform/sustain motivation during the course of the cognitively demanding CAT following surgery. Surgery was performed as described previously [58], with the following modifications. After anesthesia (isoflurane, 3.5–1% in 1.5L/min O2) and preparation of craniotomies, three 0–80 s/s screws were implanted into the skull for anchoring the cement.…”

Section: Star Methodsmentioning

confidence: 99%

Selective Attention Controls Olfactory Decisions and the Neural Encoding of Odors

et al. 2018

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Critical animal behaviors, especially among rodents, are guided by odors in remarkably well-coordinated manners, yet many extramodal sensory cues compete for cognitive resources in these ecological contexts. That rodents can engage in such odor-guided behaviors suggests that they can selectively attend to odors. Indeed, higher-order cognitive processes-such as learning, memory, decision making, and action selection-rely on the proper filtering of sensory cues based on their relative salience. We developed a behavioral paradigm to reveal that rats are capable of selectively attending to odors in the presence of competing extramodal stimuli. We found that this selective attention facilitates accurate odor-guided decisions, which become further strengthened with experience. Further, we uncovered that selective attention to odors adaptively sharpens their representation among neurons in the olfactory tubercle, an olfactory cortex region of the ventral striatum that is considered integral for evaluating sensory information in the context of motivated behaviors. Odor-directed selective attention exerts influences during moments of heightened odor anticipation and enhances odorant representation by increasing stimulus contrast in a signal-to-noise-type coding scheme. Together, these results reveal that rats engage selective attention to optimize olfactory outcomes. Further, our finding of attention-dependent coding in the olfactory tubercle challenges the notion that a thalamic relay is integral for the attentional control of sensory coding.

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“…As presented above, odorant presentation often leads to a gamma decrease coupled to a beta increase suggesting that the two rhythms share a common cellular substrate. If this is easily noticeable during odor-reward learning tasks, some studies involving passive and non-reinforced odor presentations find both gamma and beta enhancement during odor sampling (Lowry and Kay, 2007; Carlson et al, 2014). Stimulus delivery, not constraint by a nose poke may not be continuous, which could explain this discrepancy.…”

Section: Network Sustaining Beta and Gamma Rhythms In The Olfactory Bulbmentioning

confidence: 99%

“…They have been recorded in many distant brain structures related to olfactory-driven behavior. Beyond the MOB and the PCx, they have been found in the lateral entorhinal cortex (Martin et al, 2004a; Igarashi et al, 2014), in the tubercle (Carlson et al, 2014), the hippocampus (Martin et al, 2007; Igarashi et al, 2014), in motor cortex M1 (Hermer-Vazquez et al, 2007) in different parts of the prefrontal cortex (infralimbic and orbito-frontal cortex), the basolateral amygdala, and the insular cortex (Chapuis et al, 2009). Interestingly, using an olfactory discrimination Go/No-Go task, van Wingerden et al (2010) reported an increase in gamma oscillations in the orbitofrontal cortex, where power was correlated with rat training and performance, as shown by Beshel et al (2007) in the MOB.…”

Section: Gamma and Beta Oscillations Local Vs Distal Network?mentioning

confidence: 99%

Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks?

Martin

Ravel

2014

Front. Behav. Neurosci.

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Olfactory processing in behaving animals, even at early stages, is inextricable from top down influences associated with odor perception. The anatomy of the olfactory network (olfactory bulb, piriform, and entorhinal cortices) and its unique direct access to the limbic system makes it particularly attractive to study how sensory processing could be modulated by learning and memory. Moreover, olfactory structures have been early reported to exhibit oscillatory population activities easy to capture through local field potential recordings. An attractive hypothesis is that neuronal oscillations would serve to “bind” distant structures to reach a unified and coherent perception. In relation to this hypothesis, we will assess the functional relevance of different types of oscillatory activity observed in the olfactory system of behaving animals. This review will focus primarily on two types of oscillatory activities: beta (15–40 Hz) and gamma (60–100 Hz). While gamma oscillations are dominant in the olfactory system in the absence of odorant, both beta and gamma rhythms have been reported to be modulated depending on the nature of the olfactory task. Studies from the authors of the present review and other groups brought evidence for a link between these oscillations and behavioral changes induced by olfactory learning. However, differences in studies led to divergent interpretations concerning the respective role of these oscillations in olfactory processing. Based on a critical reexamination of those data, we propose hypotheses on the functional involvement of beta and gamma oscillations for odor perception and memory.

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Odor- and state-dependent olfactory tubercle local field potential dynamics in awake rats

Cited by 23 publications

References 88 publications

Olfactory tubercle stimulation alters odor preference behavior and recruits forebrain reward and motivational centers

Olfactory tubercle stimulation alters odor preference behavior and recruits forebrain reward and motivational centers

Selective Attention Controls Olfactory Decisions and the Neural Encoding of Odors

Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks?

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