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Motivational states activate distinct hippocampal representations to guide goal-directed behaviors.

ABSTRACT: Adaptive behaviors are guided by motivation and memory. Motivational states specify goals, and memory can inform motivated behavior by providing detailed records of past experiences when goals were obtained. These 2 fundamental processes interact to guide animals to biologically relevant targets, but the neuronal mechanisms that integrate them remain unknown. To investigate these mechanisms, we recorded unit activity from the same population of hippocampal neurons as rats performed identical tasks while either food or water deprived. We compared the influence of motivational state (hunger and thirst), memory demand, and spatial behavior in 2 tasks: hippocampus-dependent contextual memory retrieval and hippocampus-independent random foraging. We found that: (i) hippocampal coding was most strongly influenced by motivational state during contextual memory retrieval, when motivational cues were required to select among remembered, goal-directed actions in the same places; (ii) the same neuronal populations were relatively unaffected by motivational state during random foraging, when hunger and thirst were incidental to behavior, and signals derived from deprivation states thus informed, but did not determine, hippocampal coding; and (iii) "prospective coding" in the contextual retrieval task was not influenced by allocentric spatial trajectory, but rather by the animal's deprivation state and the associated, non-spatial target, suggesting that hippocampal coding includes a wide range of predictive associations. The results show that beyond coding spatiotemporal context, hippocampal representations encode the relationships between internal states, the external environment, and action to provide a mechanism by which motivation and memory are coordinated to guide behavior.

SUBMITTER: Kennedy PJ

PROVIDER: S-EPMC2705558 | biostudies-literature | 2009 Jun

REPOSITORIES: biostudies-literature

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Motivational states activate distinct hippocampal representations to guide goal-directed behaviors.

Kennedy Pamela J PJ Shapiro Matthew L ML

Proceedings of the National Academy of Sciences of the United States of America 20090615 26

Adaptive behaviors are guided by motivation and memory. Motivational states specify goals, and memory can inform motivated behavior by providing detailed records of past experiences when goals were obtained. These 2 fundamental processes interact to guide animals to biologically relevant targets, but the neuronal mechanisms that integrate them remain unknown. To investigate these mechanisms, we recorded unit activity from the same population of hippocampal neurons as rats performed identical tas ...[more]

PMID: 19528659

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Project description:The co-morbidity of anxiety and dysfunctional reward processing in illnesses such as addiction and depression suggests that common neural circuitry contributes to these disparate neuropsychiatric symptoms. The extended amygdala, including the bed nucleus of the stria terminalis (BNST), modulates fear and anxiety, but also projects to the ventral tegmental area (VTA), a region implicated in reward and aversion, thus providing a candidate neural substrate for integrating diverse emotional states. However, the precise functional connectivity between distinct BNST projection neurons and their postsynaptic targets in the VTA, as well as the role of this circuit in controlling motivational states, have not been described. Here we record and manipulate the activity of genetically and neurochemically identified VTA-projecting BNST neurons in freely behaving mice. Collectively, aversive stimuli exposure produced heterogeneous firing patterns in VTA-projecting BNST neurons. By contrast, in vivo optically identified glutamatergic projection neurons displayed a net enhancement of activity to aversive stimuli, whereas the firing rate of identified GABAergic (?-aminobutyric acid-containing) projection neurons was suppressed. Channelrhodopsin-2-assisted circuit mapping revealed that both BNST glutamatergic and GABAergic projections preferentially innervate postsynaptic non-dopaminergic VTA neurons, thus providing a mechanistic framework for in vivo circuit perturbations. In vivo photostimulation of BNST glutamatergic projections resulted in aversive and anxiogenic behavioural phenotypes. Conversely, activation of BNST GABAergic projections produced rewarding and anxiolytic phenotypes, which were also recapitulated by direct inhibition of VTA GABAergic neurons. These data demonstrate that functionally opposing BNST to VTA circuits regulate rewarding and aversive motivational states, and may serve as a crucial circuit node for bidirectionally normalizing maladaptive behaviours.

Project description:UnlabelledThe basal ganglia (BG) control action selection, motor programs, habits, and goal-directed learning. The striatum, the principal input structure of BG, is predominantly composed of medium-sized spiny neurons (MSNs). Arising from these spatially intermixed MSNs, two inhibitory outputs form two main efferent pathways, the direct and indirect pathways. Striatonigral MSNs give rise to the activating, direct pathway MSNs and striatopallidal MSNs to the inhibitory, indirect pathway (iMSNs). BG output nuclei integrate information from both pathways to fine-tune motor procedures and to acquire complex habits and skills. Therefore, balanced activity between both pathways is crucial for harmonious functions of the BG. Despite the increase in knowledge concerning the role of glutamate NMDA receptors (NMDA-Rs) in the striatum, understanding of the specific functions of NMDA-R iMSNs is still lacking. For this purpose, we generated a conditional knock-out mouse to address the functions of the NMDA-R in the indirect pathway. At the cellular level, deletion of GluN1 in iMSNs leads to a reduction in the number and strength of the excitatory corticostriatopallidal synapses. The subsequent scaling down in input integration leads to dysfunctional changes in BG output, which is seen as reduced habituation, delay in goal-directed learning, lack of associative behavior, and impairment in action selection or skill learning. The NMDA-R deletion in iMSNs causes a decrease in the synaptic strength of striatopallidal neurons, which in turn might lead to a imbalanced integration between direct and indirect MSN pathways, making mice less sensitive to environmental change. Therefore, their ability to learn and adapt to the environment-based experience was significantly affected.Significance statementThe striatum controls habits, locomotion, and goal-directed behaviors by coordinated activation of two antagonistic pathways. Insofar as NMDA receptors (NMDA-Rs) play a key role in synaptic plasticity essential for sustaining these behaviors, we generated a mouse model lacking NMDA-Rs specifically in striatopallidal neurons. To our knowledge, this is the first time that a specific deletion of inhibitory, indirect pathway medium-sized spiny neuron (iMSN) NMDA-Rs has been used to address the role of these receptors in the inhibitory pathway. Importantly, we found that this specific deletion led to a significant reduction in the number and strength of the cortico-iMSN synapses, which resulted in the significant impairments of behaviors orchestrated by the basal ganglia. Our findings indicate that the NMDA-Rs of the indirect pathway are essential for habituation, action selection, and goal-directed learning.

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Motivational states activate distinct hippocampal representations to guide goal-directed behaviors.

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Motivational states activate distinct hippocampal representations to guide goal-directed behaviors.

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