During visually guided behavior, the prefrontal cortex plays a pivotal role in mapping sensory inputs onto appropriate motor plans. When the sensory input is ambiguous, this involves deliberation. It is not known whether the deliberation is implemented as a competition between possible stimulus interpretations or between possible motor plans. Here we study neural population activity in the prefrontal cortex of macaque monkeys trained to flexibly report perceptual judgments of ambiguous visual stimuli. We find that the population activity initially represents the formation of a perceptual choice before transitioning into the representation of the motor plan. Stimulus strength and prior expectations both bear on the formation of the perceptual choice, but not on the formation of the action plan. These results suggest that prefrontal circuits involved in action selection are also used for the deliberation of abstract propositions divorced from a specific motor plan, thus providing a crucial mechanism for abstract reasoning.
Decisions as to whether to continue with an ongoing activity or to switch to an alternative are a constant in an animal’s natural world, and in particular underlie foraging behavior and performance in food preference tests. Stimuli experienced by the animal both impact the choice and are themselves impacted by the choice, in a dynamic back and forth. Here, we present model neural circuits, based on spiking neurons, in which the choice to switch away from ongoing behavior instantiates this back and forth, arising as a state transition in neural activity. We analyze two classes of circuit, which differ in whether state transitions result from a loss of hedonic input from the stimulus (an “entice to stay” model) or from aversive stimulus-input (a “repel to leave” model). In both classes of model, we find that the mean time spent sampling a stimulus decreases with increasing value of the alternative stimulus, a fact that we linked to the inclusion of depressing synapses in our model. The competitive interaction is much greater in “entice to stay” model networks, which has qualitative features of the marginal value theorem, and thereby provides a framework for optimal foraging behavior. We offer suggestions as to how our models could be discriminatively tested through the analysis of electrophysiological and behavioral data.
more » « less- Award ID(s):
- 2011846
- NSF-PAR ID:
- 10506774
- Editor(s):
- Soltani, Alireza
- Publisher / Repository:
- Ruth Nussinov
- Date Published:
- Journal Name:
- PLOS Computational Biology
- Volume:
- 17
- Issue:
- 9
- ISSN:
- 1553-7358
- Page Range / eLocation ID:
- e1009012
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract -
Survival relies on the ability to flexibly choose between different actions according to varying environmental circumstances. Many lines of evidence indicate that action selection involves signaling in corticostriatal circuits, including the orbitofrontal cortex (OFC) and dorsomedial striatum (DMS). While choice-specific responses have been found in individual neurons from both areas, it is unclear whether populations of OFC or DMS neurons are better at encoding an animal’s choice. To address this, we trained head-fixed mice to perform an auditory guided two-alternative choice task, which required moving a joystick forward or backward. We then used silicon microprobes to simultaneously measure the spiking activity of OFC and DMS ensembles, allowing us to directly compare population dynamics between these areas within the same animals. Consistent with previous literature, both areas contained neurons that were selective for specific stimulus-action associations. However, analysis of concurrently recorded ensemble activity revealed that the animal’s trial-by-trial behavior could be decoded more accurately from DMS dynamics. These results reveal substantial regional differences in encoding action selection, suggesting that DMS neural dynamics are more specialized than OFC at representing an animal’s choice of action. NEW & NOTEWORTHY While previous literature shows that both orbitofrontal cortex (OFC) and dorsomedial striatum (DMS) represent information relevant to selecting specific actions, few studies have directly compared neural signals between these areas. Here we compared OFC and DMS dynamics in mice performing a two-alternative choice task. We found that the animal’s choice could be decoded more accurately from DMS population activity. This work provides among the first evidence that OFC and DMS differentially represent information about an animal’s selected action.more » « less
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We aimed to examine mechanistically the observed foraging differences across two honey bee, Apis mellifera , subspecies using the proboscis extension response assay. Specifically, we compared differences in appetitive reversal learning ability between honey bee subspecies: Apis mellifera caucasica (Pollman), and Apis mellifera syriaca (Skorikov) in a “common garden” apiary. It was hypothesized that specific learning differences could explain previously observed foraging behavior differences of these subspecies: A.m. caucasica switches between different flower color morphs in response to reward variability, and A.m. syriaca does not switch. We suggest that flower constancy allows reduced exposure by minimizing search and handling time, whereas plasticity is important when maximizing harvest in preparation for long winter is at a premium. In the initial or Acquisition phase of the test we examined specifically discrimination learning, where bees were trained to respond to a paired conditioned stimulus with an unconditioned stimulus and not to respond to a second conditioned stimulus that is not followed by an unconditioned stimulus. We found no significant differences among the subspecies in the Acquisition phase in appetitive learning. During the second, Reversal phase of the experiment, where flexibility in association was tested, the paired and unpaired conditioned stimuli were reversed. During the Reversal phase A.m. syriaca showed a reduced ability to learn the reverse association in the appetitive learning task. This observation is consistent with the hypothesis that A.m. syriaca foragers cannot change the foraging choice because of lack of flexibility in appetitive associations under changing contingencies. Interestingly, both subspecies continued responding to the previously rewarded conditioned stimulus in the reversal phase. We discuss potential ecological correlates and molecular underpinnings of these differences in learning across the two subspecies. In addition, in a supplemental experiment we demonstrated that these differences in appetitive reversal learning do not occur in other learning contexts.more » « less
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To adapt to their environments, animals must generate behaviors that are closely aligned to a rapidly changing sensory world. However, behavioral states such as foraging or courtship typically persist over long time scales to ensure proper execution. It remains unclear how neural circuits generate persistent behavioral states while maintaining the flexibility to select among alternative states when the sensory context changes. Here, we elucidate the functional architecture of a neural circuit controlling the choice between roaming and dwelling states, which underlie exploration and exploitation during foraging in C. elegans . By imaging ensemble-level neural activity in freely moving animals, we identify stereotyped changes in circuit activity corresponding to each behavioral state. Combining circuit-wide imaging with genetic analysis, we find that mutual inhibition between two antagonistic neuromodulatory systems underlies the persistence and mutual exclusivity of the neural activity patterns observed in each state. Through machine learning analysis and circuit perturbations, we identify a sensory processing neuron that can transmit information about food odors to both the roaming and dwelling circuits and bias the animal towards different states in different sensory contexts, giving rise to context-appropriate state transitions. Our findings reveal a potentially general circuit architecture that enables flexible, sensory-driven control of persistent behavioral states.more » « less
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Abstract Perception reflects not only sensory inputs, but also the endogenous state when these inputs enter the brain. Prior studies show that endogenous neural states influence stimulus processing through non-specific, global mechanisms, such as spontaneous fluctuations of arousal. It is unclear if endogenous activity influences circuit and stimulus-specific processing and behavior as well. Here we use intracranial recordings from 30 pre-surgical epilepsy patients to show that patterns of endogenous activity are related to the strength of trial-by-trial neural tuning in different visual category-selective neural circuits. The same aspects of the endogenous activity that relate to tuning in a particular neural circuit also correlate to behavioral reaction times only for stimuli from the category that circuit is selective for. These results suggest that endogenous activity can modulate neural tuning and influence behavior in a circuit- and stimulus-specific manner, reflecting a potential mechanism by which endogenous neural states facilitate and bias perception.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1371/journal.pcbi.1009012
