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

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          Abstract

          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.

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          Most cited references71

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          Cognitive maps in rats and men.

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            Spontaneous behaviors drive multidimensional, brainwide activity

            Neuronal populations in sensory cortex produce variable responses to sensory stimuli and exhibit intricate spontaneous activity even without external sensory input. Cortical variability and spontaneous activity have been variously proposed to represent random noise, recall of prior experience, or encoding of ongoing behavioral and cognitive variables. Recording more than 10,000 neurons in mouse visual cortex, we observed that spontaneous activity reliably encoded a high-dimensional latent state, which was partially related to the mouse’s ongoing behavior and was represented not just in visual cortex but also across the forebrain. Sensory inputs did not interrupt this ongoing signal but added onto it a representation of external stimuli in orthogonal dimensions. Thus, visual cortical population activity, despite its apparently noisy structure, reliably encodes an orthogonal fusion of sensory and multidimensional behavioral information.
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              Single-trial neural dynamics are dominated by richly varied movements

              When experts are immersed in a task, do their brains prioritize task-related activity? Most efforts to understand neural activity during well-learned tasks focus on cognitive computations and task-related movements. We wondered whether task-performing animals explore a broader movement landscape, and how this impacts neural activity. We characterized movements using video and other sensors and measured neural activity using widefield and two-photon imaging. Cortex-wide activity was dominated by movements, especially uninstructed movements not required for the task. Some uninstructed movements were aligned to trial events. Accounting for them revealed that neurons with similar trial-averaged activity often reflected utterly different combinations of cognitive and movement variables. Other movements occurred idiosyncratically, accounting for trial-by-trial fluctuations that are often considered “noise”. This held true throughout task-learning and for extracellular Neuropixels recordings that included subcortical areas. Our observations argue that animals execute expert decisions while performing richly varied, uninstructed movements that profoundly shape neural activity.
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                Author and article information

                Contributors
                Journal
                IBRO Neurosci Rep
                IBRO Neurosci Rep
                IBRO Neuroscience Reports
                Elsevier
                2667-2421
                24 May 2022
                December 2022
                24 May 2022
                : 13
                : 9-14
                Affiliations
                [a ]Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD, USA
                [b ]The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD, USA
                [c ]Department of Biomedical Engineering, School of Engineering, Johns Hopkins University, Baltimore, MD, USA
                Author notes
                [* ]Corresponding author. smoorec2@ 123456jhu.edu
                [** ]Corresponding author at: Department of Psychological and Brain Sciences, Krieger School of Arts and Sciences, Johns Hopkins University, Baltimore, MD, USA. kkuchib1@ 123456jhu.edu
                Article
                S2667-2421(22)00036-7
                10.1016/j.ibneur.2022.05.006
                9163689
                35669385
                8eb54a2e-8dd5-4079-a6f8-3d48ad7fbd47
                © 2022 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 18 February 2022
                : 20 May 2022
                : 23 May 2022
                Categories
                Articles from the Latin America Mini Series

                learning,instrumental learning,behavior,systems neuroscience,large-scale recordings,big data,goal-directed learning,circuit,stimulus-response,acquisition

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