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The nucleus accumbens: a switchboard for goal-directed behaviors.

Gruber AJ, Hussain RJ, O'Donnell P - PLoS ONE (2009)

Bottom Line: The prefrontal cortex (PFC) and associated basal ganglia circuits are likely candidates as neural structures responsible for such balance, while the hippocampus may be responsible for spatial/contextual information.Neural firing and local field potentials in the NA core synchronized with hippocampal activity during spatial exploration, but during lever pressing they instead synchronized more strongly with the PFC.Thus, the ability to switch synchronization in a task-dependent manner indicates that the NA core can dynamically select its inputs to suit environmental demands, thereby contributing to decision-making, a function that was thought to primarily depend on the PFC.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America.

ABSTRACT
Reward intake optimization requires a balance between exploiting known sources of rewards and exploring for new sources. The prefrontal cortex (PFC) and associated basal ganglia circuits are likely candidates as neural structures responsible for such balance, while the hippocampus may be responsible for spatial/contextual information. Although studies have assessed interactions between hippocampus and PFC, and between hippocampus and the nucleus accumbens (NA), it is not known whether 3-way interactions among these structures vary under different behavioral conditions. Here, we investigated these interactions with multichannel recordings while rats explored an operant chamber and while they performed a learned lever-pressing task for reward in the same chamber shortly afterward. Neural firing and local field potentials in the NA core synchronized with hippocampal activity during spatial exploration, but during lever pressing they instead synchronized more strongly with the PFC. The latter is likely due to transient drive of NA neurons by bursting prefrontal activation, as in vivo intracellular recordings in anesthetized rats revealed that NA up states can transiently synchronize with spontaneous PFC activity and PFC stimulation with a bursting pattern reliably evoked up states in NA neurons. Thus, the ability to switch synchronization in a task-dependent manner indicates that the NA core can dynamically select its inputs to suit environmental demands, thereby contributing to decision-making, a function that was thought to primarily depend on the PFC.

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PFC-NA unit correlation is strengthened during bar press for a natural reward.(A) Representative cross-correlograms of a NA-PFC neuron pair (referenced to PFC firing at time 0) when the animal was exploring (gray) and during bar pressing for sucrose (black). Right: bar graphs showing the ratio between the crosscorrelogram peak and a similar analysis of shuffled recordings from the same pairs for both behavioral conditions. Mean±SD; * p<0.05 by paired t test. (B) Similar cross-correlation of a representative VH-NA pair during exploration (gray) and bar pressing (red). No differences were observed in these cases.
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pone-0005062-g001: PFC-NA unit correlation is strengthened during bar press for a natural reward.(A) Representative cross-correlograms of a NA-PFC neuron pair (referenced to PFC firing at time 0) when the animal was exploring (gray) and during bar pressing for sucrose (black). Right: bar graphs showing the ratio between the crosscorrelogram peak and a similar analysis of shuffled recordings from the same pairs for both behavioral conditions. Mean±SD; * p<0.05 by paired t test. (B) Similar cross-correlation of a representative VH-NA pair during exploration (gray) and bar pressing (red). No differences were observed in these cases.

Mentions: We recorded single-unit activity simultaneously in the NA, VH and PFC in awake, freely moving rats using chronically implanted electrode arrays. Recordings were carried out during two different behavioral conditions in the same session: first, when rats were exploring the test chamber during the initial 5–10 minutes of recording while the lever was retracted, and then during an immediately following period of 10–20 minutes when rats were required to press the extended lever in order to obtain a natural reward (sucrose). A visual cue and the lever extension indicated availability of the reward, and rats typically pressed the lever within one second. NA (49/60), PFC (30/34) and VH (8/15) neurons exhibited phasic changes in firing relative to the lever press. All the VH neurons that responded showed an increase in firing following the lever press; in the NA and PFC, units exhibited increases or decreases in firing associated with the lever press or with the reward delivery, as previously reported [20], [27] (Figure S1, Table S1). We then assessed whether synchronization between neurons across brain regions changed with the behavioral state by constructing cross-correlograms of neural responses during lever presses and during epochs of the exploration phase in which rats were moving toward and making contact with the lever port. These epochs of the exploration phase were confirmed by video recordings of rats in the chamber, and were chosen so that spatial information was similar in both behavioral conditions. For this analysis, we included units from the three animals in which single unit responses were recorded in all three regions simultaneously. Each NA unit used in a HC-NA comparison was also used in a PFC-NA comparison so as to provide a within-subject control. Likewise, data for the two behavioral conditions are from the same session, providing a within-session control. All NA-PFC pairs tested (n = 8) showed enhanced correlation during the bar press compared to the exploratory period (Figure 1A). The strength of the correlation was calculated by determining the ratio between crosscorrelogram peaks and shuffled crosscorrelograms. For NA-PFC pairs, this ratio was 1.33±0.36 during the exploratory stage and increased to 1.67±0.40 during bar press (n = 8; p = 0.014, paired t test). The correlation between NA and VH neurons did not differ between exploration and the instrumental task (1.60±0.72 during exploration; 1.70±0.70 during bar press; n = 5; p = 0.37, paired t test; Figure 1B). Power analysis revealed 77% confidence for the NA-PFC relationship and 92% confidence for the HC-NA relationship, indicating robust power despite the limited number of simultaneous single-unit recordings. Thus, lever-pressing behavior was associated with a stronger PFC-NA correlation in neuronal firing than spatial exploration.


The nucleus accumbens: a switchboard for goal-directed behaviors.

Gruber AJ, Hussain RJ, O'Donnell P - PLoS ONE (2009)

PFC-NA unit correlation is strengthened during bar press for a natural reward.(A) Representative cross-correlograms of a NA-PFC neuron pair (referenced to PFC firing at time 0) when the animal was exploring (gray) and during bar pressing for sucrose (black). Right: bar graphs showing the ratio between the crosscorrelogram peak and a similar analysis of shuffled recordings from the same pairs for both behavioral conditions. Mean±SD; * p<0.05 by paired t test. (B) Similar cross-correlation of a representative VH-NA pair during exploration (gray) and bar pressing (red). No differences were observed in these cases.
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Related In: Results  -  Collection

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pone-0005062-g001: PFC-NA unit correlation is strengthened during bar press for a natural reward.(A) Representative cross-correlograms of a NA-PFC neuron pair (referenced to PFC firing at time 0) when the animal was exploring (gray) and during bar pressing for sucrose (black). Right: bar graphs showing the ratio between the crosscorrelogram peak and a similar analysis of shuffled recordings from the same pairs for both behavioral conditions. Mean±SD; * p<0.05 by paired t test. (B) Similar cross-correlation of a representative VH-NA pair during exploration (gray) and bar pressing (red). No differences were observed in these cases.
Mentions: We recorded single-unit activity simultaneously in the NA, VH and PFC in awake, freely moving rats using chronically implanted electrode arrays. Recordings were carried out during two different behavioral conditions in the same session: first, when rats were exploring the test chamber during the initial 5–10 minutes of recording while the lever was retracted, and then during an immediately following period of 10–20 minutes when rats were required to press the extended lever in order to obtain a natural reward (sucrose). A visual cue and the lever extension indicated availability of the reward, and rats typically pressed the lever within one second. NA (49/60), PFC (30/34) and VH (8/15) neurons exhibited phasic changes in firing relative to the lever press. All the VH neurons that responded showed an increase in firing following the lever press; in the NA and PFC, units exhibited increases or decreases in firing associated with the lever press or with the reward delivery, as previously reported [20], [27] (Figure S1, Table S1). We then assessed whether synchronization between neurons across brain regions changed with the behavioral state by constructing cross-correlograms of neural responses during lever presses and during epochs of the exploration phase in which rats were moving toward and making contact with the lever port. These epochs of the exploration phase were confirmed by video recordings of rats in the chamber, and were chosen so that spatial information was similar in both behavioral conditions. For this analysis, we included units from the three animals in which single unit responses were recorded in all three regions simultaneously. Each NA unit used in a HC-NA comparison was also used in a PFC-NA comparison so as to provide a within-subject control. Likewise, data for the two behavioral conditions are from the same session, providing a within-session control. All NA-PFC pairs tested (n = 8) showed enhanced correlation during the bar press compared to the exploratory period (Figure 1A). The strength of the correlation was calculated by determining the ratio between crosscorrelogram peaks and shuffled crosscorrelograms. For NA-PFC pairs, this ratio was 1.33±0.36 during the exploratory stage and increased to 1.67±0.40 during bar press (n = 8; p = 0.014, paired t test). The correlation between NA and VH neurons did not differ between exploration and the instrumental task (1.60±0.72 during exploration; 1.70±0.70 during bar press; n = 5; p = 0.37, paired t test; Figure 1B). Power analysis revealed 77% confidence for the NA-PFC relationship and 92% confidence for the HC-NA relationship, indicating robust power despite the limited number of simultaneous single-unit recordings. Thus, lever-pressing behavior was associated with a stronger PFC-NA correlation in neuronal firing than spatial exploration.

Bottom Line: The prefrontal cortex (PFC) and associated basal ganglia circuits are likely candidates as neural structures responsible for such balance, while the hippocampus may be responsible for spatial/contextual information.Neural firing and local field potentials in the NA core synchronized with hippocampal activity during spatial exploration, but during lever pressing they instead synchronized more strongly with the PFC.Thus, the ability to switch synchronization in a task-dependent manner indicates that the NA core can dynamically select its inputs to suit environmental demands, thereby contributing to decision-making, a function that was thought to primarily depend on the PFC.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy & Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland, United States of America.

ABSTRACT
Reward intake optimization requires a balance between exploiting known sources of rewards and exploring for new sources. The prefrontal cortex (PFC) and associated basal ganglia circuits are likely candidates as neural structures responsible for such balance, while the hippocampus may be responsible for spatial/contextual information. Although studies have assessed interactions between hippocampus and PFC, and between hippocampus and the nucleus accumbens (NA), it is not known whether 3-way interactions among these structures vary under different behavioral conditions. Here, we investigated these interactions with multichannel recordings while rats explored an operant chamber and while they performed a learned lever-pressing task for reward in the same chamber shortly afterward. Neural firing and local field potentials in the NA core synchronized with hippocampal activity during spatial exploration, but during lever pressing they instead synchronized more strongly with the PFC. The latter is likely due to transient drive of NA neurons by bursting prefrontal activation, as in vivo intracellular recordings in anesthetized rats revealed that NA up states can transiently synchronize with spontaneous PFC activity and PFC stimulation with a bursting pattern reliably evoked up states in NA neurons. Thus, the ability to switch synchronization in a task-dependent manner indicates that the NA core can dynamically select its inputs to suit environmental demands, thereby contributing to decision-making, a function that was thought to primarily depend on the PFC.

Show MeSH