Revealing abrupt transitions from goal-directed to habitual behavior.

A fundamental tenet of animal behavior is that decision-making involves multiple 'controllers.' Initially, behavior is goal-directed, driven by desired outcomes, shifting later to habitual control, where cues trigger actions independent of motivational state. Clark Hull's question from 1943 still resonates today: "Is this transition abrupt, or is it gradual and progressive?"1 Despite a century-long belief in gradual transitions, this question remains unanswered2,3 as current methods cannot disambiguate goal-directed versus habitual control in real-time. Here, we introduce a novel 'volitional engagement' approach, motivating animals by palatability rather than biological need. Offering less palatable water in the home cage4,5 reduced motivation to 'work' for plain water in an auditory discrimination task when compared to water-restricted animals. Using quantitative behavior and computational modeling6, we found that palatability-driven animals learned to discriminate as quickly as water-restricted animals but exhibited state-like fluctuations when responding to the reward-predicting cue-reflecting goal-directed behavior. These fluctuations spontaneously and abruptly ceased after thousands of trials, with animals now always responding to the reward-predicting cue. In line with habitual control, post-transition behavior displayed motor automaticity, decreased error sensitivity (assessed via pupillary responses), and insensitivity to outcome devaluation. Bilateral lesions of the habit-related dorsolateral striatum7 blocked transitions to habitual behavior. Thus, 'volitional engagement' reveals spontaneous and abrupt transitions from goal-directed to habitual behavior, suggesting the involvement of a higher-level process that arbitrates between the two.

Slow or sudden: Re-interpreting the learning curve for modern systems neuroscience.

Learning is fundamental to animal survival. Animals must learn to link sensory cues in the environment to actions that lead to reward or avoid punishment. Rapid learning can then be highly adaptive and the difference between life or death. To explore the neural dynamics and circuits that underlie learning, however, has typically required the use of laboratory paradigms with tight control of stimuli, action sets, and outcomes. Learning curves in such reward-based tasks are reported as slow and gradual, with animals often taking hundreds to thousands of trials to reach expert performance. The slow, highly variable, and incremental learning curve remains the largely unchallenged belief in modern systems neuroscience. Here, we provide historical and contemporary evidence that instrumental forms of reward-learning can be dissociated into two parallel processes: knowledge acquisition which is rapid with step-like improvements, and behavioral expression which is slower and more variable. We further propose that this conceptual distinction may allow us to isolate the associative (knowledge-related) and non-associative (performance-related) components that influence learning. We then discuss the implications that this revised understanding of the learning curve has for systems neuroscience.

Extrasynaptic Communication.

Streams of action potentials or long depolarizations evoke a massive exocytosis of transmitters and peptides from the surface of dendrites, axons and cell bodies of different neuron types. Such mode of exocytosis is known as extrasynaptic for occurring without utilization of synaptic structures. Most transmitters and all peptides can be released extrasynaptically. Neurons may discharge their contents with relative independence from the axon, soma and dendrites. Extrasynaptic exocytosis takes fractions of a second in varicosities or minutes in the soma or dendrites, but its effects last from seconds to hours. Unlike synaptic exocytosis, which is well localized, extrasynaptic exocytosis is diffuse and affects neuronal circuits, glia and blood vessels. Molecules that are liberated may reach extrasynaptic receptors microns away. The coupling between excitation and exocytosis follows a multistep mechanism, different from that at synapses, but similar to that for the release of hormones. The steps from excitation to exocytosis have been studied step by step for the vital transmitter serotonin in leech Retzius neurons. The events leading to serotonin exocytosis occur similarly for the release of other transmitters and peptides in central and peripheral neurons. Extrasynaptic exocytosis occurs commonly onto glial cells, which react by releasing the same or other transmitters. In the last section, we discuss how illumination of the retina evokes extrasynaptic release of dopamine and ATP. Dopamine contributes to light-adaptation; ATP activates glia, which mediates an increase in blood flow and oxygenation. A proper understanding of the workings of the nervous system requires the understanding of extrasynaptic communication.

A role of oligodendrocytes in information processing.

Myelinating oligodendrocytes enable fast propagation of action potentials along the ensheathed axons. In addition, oligodendrocytes play diverse non-canonical roles including axonal metabolic support and activity-dependent myelination. An open question remains whether myelination also contributes to information processing in addition to speeding up conduction velocity. Here, we analyze the role of myelin in auditory information processing using paradigms that are also good predictors of speech understanding in humans. We compare mice with different degrees of dysmyelination using acute multiunit recordings in the auditory cortex, in combination with behavioral readouts. We find complex alterations of neuronal responses that reflect fatigue and temporal acuity deficits. We observe partially discriminable but similar deficits in well myelinated mice in which glial cells cannot fully support axons metabolically. We suggest a model in which myelination contributes to sustained stimulus perception in temporally complex paradigms, with a role of metabolically active oligodendrocytes in cortical information processing.

Strategies of locomotion composition.

This review aims to highlight the importance of saccades during locomotion as a strategy to reduce sensory information loss while the subject is moving. Acquiring sensory data from the environment during movement results in a temporal flow of information, as the sensory precept changes with the position of the observer. Accordingly, the movement pattern shapes the sensory flow. Therefore, the requirements of locomotion and sensation have to be balanced in the behaviour of the organism. Insect vision provides deep insight into the interplay between action and perception. Insects can shape their optic flow by reducing their rotational movements to fast and short saccades. This generates prolonged phases of translations which provide depth information. Extensive behavioural and physiological studies on insects show how shaping the optic flow facilitates the coding of motion vision. Indeed the saccadic strategy provides an elegant solution to optimise sensory flow. Complementary studies in other taxa reported similar locomotion strategies emphasising the crucial influence of sensory flow on locomotion.