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Neuronal Roles in Smell and Reward Processing

Study reveals how basal forebrain neurons impact decision-making and smell recognition.

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Our behavior and attention can strongly affect how our brain processes information. This can range from how we perceive things around us to how we think, learn, and remember. A specific area in the brain called the basal forebrain (BF) plays a key role in regulating our behaviors and attention. It helps control our focus, sensory processing, feeding, Rewards, arousal, and learning. When these brain circuits deteriorate, it can lead to memory and cognitive problems in diseases.

Research shows that the BF adjusts its activity based on expected rewards. For instance, when we expect a reward, our brain's response to sensory information changes. If certain cells in the BF are inhibited, it can affect our attention to important stimuli. Interestingly, two types of BF Neurons, called PV (parvalbumin) and SST (somatostatin) neurons, behave differently when it comes to learning from rewards. To find out how these neuron types affect our perception and decision-making, researchers studied their activity patterns in different situations.

The Mouse Olfactory System as a Model

The mouse's sense of smell is a good model for studying how BF influences behavior and decision-making. Specifically, both the olfactory bulb and olfactory cortex receive input from BF neurons. Mice can be trained to distinguish between different smells, making it easy to test their decision-making abilities.

When researchers examined how BF neurons influenced odor processing, they found that inhibiting certain BF neurons could impair the mice's ability to recognize different smells. Moreover, both PV and SST BF neurons showed different activities when responding to smells and rewards. This suggests that to truly understand how BF circuits affect behavior, it's essential to analyze the specific activities of these neuron types during various behaviors.

Methodology: Observing Neuronal Activity

In the experiments, researchers used a method called fiber photometry to observe the activity of PV and SST neurons while mice performed a smell-related decision-making task. The task involved training mice to recognize one odor associated with a reward (S+) while ignoring another odor (S-). As the mice performed the task, the researchers recorded the activity of the neurons.

The data revealed that PV neurons became active when the odor was presented but decreased their activity when the reward was given. On the other hand, SST neurons showed increased activity both during odor presentation and when the reward was delivered. These contrasting responses suggest that PV and SST neurons play different roles in processing sensory information and managing behavior.

The Role of PV Neurons

The study showed that PV neurons respond consistently to odors but their activity is suppressed after the delivery of a reward. Researchers discovered that when the sensory response of PV neurons was high, the overall performance of mice in distinguishing odors was lower. This indicates that higher sensory responses from PV neurons might correlate with poorer discrimination ability.

Moreover, the researchers found that the activity of PV neurons was not linked to the mice's decision-making behavior. In essence, as the performance improved, the activity of PV neurons related to the reward diminished, suggesting that the PV neurons 'mapped' the sensory information but did not directly influence the decision-making process.

The Role of SST Neurons

In contrast, SST neurons responded actively not only to odors but also to rewards. Their response to odor stimuli did not correlate with the accuracy of odor discrimination, which differs from the activity seen in PV neurons. Interestingly, when SST neurons were manipulated through chemogenetics (a method to control neuron activity), it slightly influenced the mice's decision-making bias, making them more likely to seek rewards.

This finding indicates that while SST neurons may not directly impact the ability to discriminate odors, they do have a role in guiding reward-seeking behavior during the decision-making process.

Impact of Neuronal Manipulation on Behavior

Researchers also analyzed the effects of directly stimulating or inhibiting these neuron types during different phases of the task. By manipulating the activity of PV neurons through optogenetics-using light to control neuron behavior-they observed improvements in odor discrimination when PV neurons were inhibited during odor presentations. This suggests that suppressing the PV neurons enhances the mice's ability to differentiate between smells.

On the other hand, when the researchers inhibited SST neurons, they noticed no significant impact on the accuracy of odor discrimination, though it did change how aggressively the mice sought rewards. This emphasizes the distinct roles played by these two types of neurons in behavior.

Summary of Findings

The research highlighted unique patterns in neuronal activity among the BF's PV and SST neurons in response to smells and rewards. While both types of neurons react to odors, their responses to reward delivery are notably different. PV neurons showed decreased activity when rewards were given, while SST neurons became excited.

These findings suggest that PV neurons might reduce overall performance in discrimination tasks due to their strong sensory response, while SST neurons might help regulate the urge to seek rewards without affecting the actual ability to perceive different smells.

The overall contribution of both PV and SST neurons reflects the complexity of sensory processing and decision-making behaviors in the brain. Understanding these differences in activity may provide valuable insights into how various parts of the brain work together during decision-making processes.

The Importance of Neuronal Interactions

The interaction between different types of neurons within the BF can shape behaviors significantly. The BF contains not just PV and SST neurons, but also cholinergic neurons, which play an important role in attention and arousal. The coordinated activity of these neuron types is essential for effective decision-making and sensory processing.

When studying the BF, researchers must consider how these different neurons influence each other. For example, the inhibitory connection that SST neurons have on PV neurons can alter how sensory information is processed, potentially affecting behavior during tasks that require careful discrimination.

Implications for Neurological Disorders

Understanding the roles of different BF neurons may have important implications for treating neurological and cognitive disorders. Since the BF is vulnerable to damage in conditions like Alzheimer’s disease, insights into how different neuron types contribute to cognition can inform strategies for mitigating cognitive decline.

Targeting specific neuronal circuits or enhancing the function of certain neuron types might offer ways to improve cognition and memory in individuals with neurodegenerative diseases. This kind of research could lead to more effective interventions that enhance cognitive function and quality of life.

Conclusion

In conclusion, the study of PV and SST neurons in the basal forebrain highlights the intricate workings of the brain in processing sensory information and making decisions. By understanding how these different neurons contribute to behavior, researchers can gain insights into the underlying neural mechanisms that influence cognition and could pave the way for future treatments for cognitive impairments.

Original Source

Title: Odor and reward-evoked GABAergic neuronal activity in the basal forebrain influences olfactory-guided behavior in mice

Abstract: Sensory perception relies on the flexible detection and interpretation of stimuli across variable contexts, conditions, and behavioral states. The basal forebrain is a hub for behavioral state regulation, supplying dense cholinergic and GABAergic projections to various brain regions involved in sensory processing. Of GABAergic neurons in the basal forebrain, parvalbumin (PV) and somatostatin (SST) subtypes serve opposing roles towards regulating behavioral states. To elucidate the role of basal forebrain circuits in sensory-guided behavior, we investigated GABAergic signaling dynamics during odor-guided decision-making. We used fiber photometry to record cell type-specific basal forebrain activity during an odor discrimination task and correlated temporal patterns of PV and SST neuronal activity with olfactory task performance. We found that while both PV-expressing and SST-expressing GABAergic neurons were activated by odors, PV neurons were selectively suppressed by reward whereas SST neurons were activated. Notably, chemogenetic inhibition of BF SST neurons modestly altered decision bias to favor reward-seeking while optogenetic inhibition of BF PV neurons during odor presentations improved discrimination accuracy. Together, these results suggest that the bidirectional activity of GABAergic basal forebrain neuron subtypes distinctly influence perception and decision-making during olfactory guided behavior. SIGNIFICANCE STATEMENTThis study reveals distinct roles for basal forebrain GABAergic neurons in odor perception and odor-guided decision-making. Fiber photometry shows that basal forebrain parvalbumin-expressing neurons are selectively suppressed by rewards, while somatostatin-expressing neurons are activated, establishing the unique recruitment of these GABAergic neurons during behavioral reinforcement. Chemogenetic and optogenetic interventions demonstrate divergent roles for these neuronal subtypes in reward-seeking behavior and odor perception. This research provides new insights into how GABAergic neurons in the basal forebrain shape sensory perception and decision-making.

Authors: Elizabeth L Hanson Moss, E. K. Tantry, E. Le, K. Brandel-Ankrapp, B. R. Arenkiel

Last Update: 2024-02-14 00:00:00

Language: English

Source URL: https://www.biorxiv.org/content/10.1101/2022.09.04.506524

Source PDF: https://www.biorxiv.org/content/10.1101/2022.09.04.506524.full.pdf

Licence: https://creativecommons.org/licenses/by-nc/4.0/

Changes: This summary was created with assistance from AI and may have inaccuracies. For accurate information, please refer to the original source documents linked here.

Thank you to biorxiv for use of its open access interoperability.

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