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Butler, J. L.

Publications and source records attributed to Butler, J. L..

6 recordsLinked to original sources

Rapid value learning reveals generalized and context-dependent codes in frontal cortex

Studying how the brain represents value spans distinct methods and training histories, from neuroimaging in task-naive humans to single-neuron recordings in extensively trained non-human primates. Similar findings across fields have encouraged the untested assumption that rapidly emerging and overtrained value representations are equivalent. Here we recorded single-neuron activity in anterior cingulate cortex (ACC) and orbitofrontal cortex (OFC) as macaques learned novel cue values and chose between novel and overtrained cues. Value responses emerged within 4-7 cue presentations, matching behavioural adaptation. Yet ACC and OFC used distinct codes. ACC encoded value in a common format that generalised across training history. OFC coding was more context-dependent, with distinct subpopulations recruited by choice experience. Choice novelty was also encoded independently of value before chosen value signals emerged. During learning, ACC responses shifted from overtrained secondary reinforcers to newly predictive cues. These findings establish the necessary (rapid acquisition) and sufficient (generalised format) conditions for comparing value representations across methods, species, and training histories.

neuroscience↗

Neural signatures of model-based and model-free reinforcement learning across prefrontal cortex and striatum

Animals integrate knowledge about how the state of the environment evolves to choose actions that maximise reward. Such goal-directed behaviour - or model-based (MB) reinforcement learning (RL) - can flexibly adapt choice to changes, being thus distinct from simpler habitual - or model-free (MF) RL - strategies. Previous inactivation and neuroimaging work implicates prefrontal cortex (PFC) and the caudate striatal region in MB-RL; however, details are scarce about its implementation at the single-neuron level. Here, we recorded from two PFC regions - the dorsal anterior cingulate cortex (ACC) and dorsolateral PFC (DLPFC), and two striatal regions, caudate and putamen - while two rhesus macaques performed a sequential decision-making (two-step) task in which MB-RL involves knowledge about the statistics of reward and state transitions. All four regions, but particularly the ACC, encoded the rewards received and tracked the probabilistic state transitions that occurred. However, ACC (and to a lesser extent caudate) encoded the key variables of the task - namely the interaction between reward, transition and choice - which underlies MB decision-making. ACC and caudate neurons also encoded MB-derived estimates of choice values. Moreover, caudate value estimates of the choice options flipped when a rare transition occurred, demonstrating value update based on structural knowledge of the task. The striatal regions were unique (relative to PFC) in encoding the current and previous rewards with opposing polarities, reminiscent of dopaminergic neurons, and indicative of a MF prediction error. Our findings provide a deeper understanding of selective and temporally dissociable neural mechanisms underlying goal-directed behaviour.

neuroscience↗

Covert valuation for information sampling and choice

We use our eyes to assess the value of objects around us and carefully fixate options that we are about to choose. Neurons in the prefrontal cortex reliably encode the value of fixated options, which is essential for decision making. Yet as a decision unfolds, it remains unclear how prefrontal regions determine which option should be fixated next. Here we show that anterior cingulate cortex (ACC) encodes the value of options in the periphery to guide subsequent fixations during economic choice. In an economic decision-making task involving four simultaneously presented cues, we found rhesus macaques evaluated cues using their peripheral vision. This served two distinct purposes: subjects were more likely to fixate valuable peripheral cues, and more likely to choose valuable options whose cues were never even fixated. ACC, orbitofrontal cortex, dorsolateral prefrontal cortex, and ventromedial prefrontal cortex neurons all encoded cue value post-fixation. ACC was unique, however, in also encoding the value of cues before fixation and even cues that were never fixated. This pre-saccadic value encoding by ACC predicted which cue was next fixated during the decision process. ACC therefore conducts simultaneous processing of peripheral information to guide information sampling and choice during decision making.

neuroscience↗

Distributional reinforcement learning in prefrontal cortex

Prefrontal cortex is crucial for learning and decision-making. Classic reinforcement learning (RL) theories centre on learning the expectation of potential rewarding outcomes and explain a wealth of neural data in prefrontal cortex. Distributional RL, on the other hand, learns the full distribution of rewarding outcomes and better explains dopamine responses. Here we show distributional RL also better explains prefrontal cortical responses, suggesting it is a ubiquitous mechanism for reward-guided learning.

neuroscience↗

Complementary task representationsin hippocampus and prefrontal cortexfor generalising the structure of problems

Few situations in life are completely novel. We effortlessly generalise prior knowledge to solve novel problems, abstracting common structure and mapping it onto new sensorimotor specifics. Here we trained mice on a series of reversal learning problems that shared the same structure but had different physical implementations. Performance improved across problems, demonstrating transfer of knowledge. Neurons in medial prefrontal cortex (mPFC) maintained similar representations across multiple problems, despite their different sensorimotor correlates, whereas hippocampal (dCA1) representations were more strongly influenced by the specifics of each problem. Critically, this was true both for representations of the events that comprised each trial, and those that integrated choices and outcomes over multiple trials to guide subjects decisions. These data suggest that PFC and hippocampus play complementary roles in generalisation of knowledge, with the former abstracting the common structure among related problems, and the latter mapping this structure onto the specifics of the current situation.

neuroscience↗

Regulation by the pitcher plant Sarracenia purpurea of the structure of its inquiline food web

AO_SCPLOWBSTRACTC_SCPLOWPhytotelmata, the water-filled habitats in pitcher plants, bromeliad tanks, and tree-holes, host multitrophic food webs that are model experimental systems for studying food-web structure and dynamics. However, the plant usually is considered simply as an inert container, not as an interacting part of the food web. We used a manipulative field experiment with a response-surface design to determine effects of nutrient enrichment (multiple levels of NH4NO3, PO4, and captured prey), top predator (removed or present), and the plant itself (with or without plastic tubes inserted into the pitchers to isolate the food web from the plant) on the macrobial food web within the modified leaves ("pitchers") of the carnivorous pitcher plant Sarracenia purpurea. Connection to the plant, addition of NH4NO3 and removal of the top predator significantly increased the food webs saturation, defined as its trophic depth and number of interactions. No effects on food-web saturation resulted from addition of PO4 or supplemental prey. Plants such as S. purpurea that create phytotelmata are more than inert containers and their inhabitants are more than commensal inquilines. Rather, both the plant and the inquilines are partners in a complex network of interactions.

ecology↗