Material below summarizes the article The Neural Representation of Goal-Directed Actions and Outcomes in the Ventral Striatum's Olfactory Tubercle, published on January 13, 2016, in JNeurosci and authored by Marie A. Gadziola and Daniel W. Wesson.
Goal-directed behaviors are widespread among animals and underlie a variety of complex actions including food intake, social behavior, and even pathological conditions such as gambling and drug addiction. In order to select appropriate behavioral actions, the brain must evaluate reward-related sensory and contextual information while simultaneously considering internal motivational and emotional factors.
In this paper, we demonstrated that the olfactory tubercle, a previously underappreciated region of the ventral striatum in this context, is capable of representing reward-seeking behaviors and natural reinforcers. These results highlight the olfactory tubercle as a major component of the brain’s reward circuitry that influences goal-directed behaviors, and may be essential for understanding pathological behaviors, such as those involved in drug addiction.
The ventral striatum, containing both the nucleus accumbens and olfactory tubercle, is in a key position for evaluating reward-related information, and, in turn, influencing the motivational control and execution of appropriate behaviors. The ventral striatum receives a large collection of inputs from cortex, amygdala, hippocampus, thalamus, and midbrain dopaminergic neurons. The ventral striatum can also send information to the ventral pallidum and substantia nigra to influence motor behaviors.
While numerous studies have established that neurons within the nucleus accumbens respond to several different aspects of reward-seeking behaviors, such as instruction and conditioned cues, anticipation of rewards, and conditioned behaviors, it is not known whether the olfactory tubercle also shares this function.
Previous work, largely from other researchers, has demonstrated that the olfactory tubercle can strongly influence motivated behaviors. Lesions of the olfactory tubercle can decrease mating behaviors and innate preferences for chemical signals, such as odors and pheromones, whereas electrical stimulation of the olfactory tubercle is rewarding.
As a major target of midbrain dopaminergic neurons, the olfactory tubercle may also modulate the salience of drugs of abuse. The work of Satoshi Ikemoto at the National Institute on Drug Abuse has demonstrated that infusions of cocaine into the olfactory tubercle caused rats to spend more time in the area of a testing chamber where they received the cocaine, and that rats will choose to self-administer cocaine into the olfactory tubercle more so than into the nucleus accumbens or ventral pallidum.
Our previous work further revealed that the olfactory tubercle robustly and flexibly encodes the associated meaning of conditioned odor cues. Together, these findings suggest a critical role for the olfactory tubercle in processing reward-related information to adaptively guide behavior.
To investigate the role of olfactory tubercle neurons in representing goal-directed behaviors and natural reinforcers, such as food and water, mice were trained on an instrumental learning task, in which a particular behavior, also known as the “instrumental action,” can be strengthened by associating it with a rewarding consequence. In our study, thirsty mice learned to lick a spout for approximately 2.5 seconds (about 20 licks) in order to receive a small drop of fluid as a reward. Trials were self-initiated by the mice, and they received no instruction or predictive cues related to the task or reward delivery. Mice were also implanted with a multi-wire electrode bundle within the olfactory tubercle to obtain extracellular recordings of neuronal activity. This task structure allowed us to examine how firing rates of single neurons were modified after reward delivery, while controlling for changes in response to licking during reward consumption. Additionally, we could examine how neural activity changed during the instrumental action of licking compared to baseline levels.
A major finding from this work is that the olfactory tubercle encodes goal-directed actions. The majority of neurons increased their firing rates during instrumental licking relative to when they were not licking. While some neurons sustained this change in activity throughout the entire instrumental licking period, other neurons only briefly altered activity around the onset of licking. Interestingly, we observed that changes in neural activity occurred prior to the first instrumental lick.
To explore motivational factors that might underlie this anticipatory pre-response activity, we split the total number of trials into early and late session blocks. Three behavioral measures indicated that mice were less motivated to perform our task throughout a one hour recording session. During late session trials, mice were less thirsty, took longer to initiate trials, and licked for less time after reward delivery. When comparing neural activity in late versus early session trials, we found that the pre-response activity was more prominent and occurred earlier relative to the first lick during late session trials when mice were less motivated. This raises an interesting possibility that when motivational drive is lower, more activity within the olfactory tubercle is required to invigorate continued performance of the task.
An additional major finding is that olfactory tubercle neurons encode rewards. Olfactory tubercle neurons not only responded to natural reinforcers, but some neurons were differentially modulated by rewards of different sizes or types. On one experimental session, we randomized the presentation of water rewards at three different volumes. Olfactory tubercle neurons were more responsive and showed a greater increase in firing rate in response to larger rewards. During a different experimental session, we randomized the presentation of three different rewards: water, saccharin (a sweet, high palatability solution), and quinine (a bitter, low palatability solution) at two different volumes. We found that olfactory tubercle neurons were differentially modulated by the different types of rewards. Whereas some neurons responded to many of the rewards, a subset of neurons were highly selective and only altered firing rates in response to a single reward type. These highly selective neurons were more likely to respond to the saccharine reward, suggesting that olfactory tubercle neurons are sensitive to palatability features.
This work is the first demonstration that the olfactory tubercle represents instrumental actions and natural reinforcers. This research highlights that more regions of the ventral striatum are participating in reward-guided behavior than simply the nucleus accumbens, and that the olfactory tubercle should be more regularly included in neural models of the reward circuitry.
Future studies should aim to achieve a more complete understanding of ventral striatum functioning in the context of reward-guided behaviors.
The Neural Representation of Goal-Directed Actions and Outcomes in the Ventral Striatum's Olfactory Tubercle. Marie Gadziola and Daniel Wesson. The Journal of Neuroscience Jan 2016, 36(2): 548-560; DOI: 10.1523/JNEUROSCI.3328-15.2016