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      Bias in Prestimulus Motor Cortical Activity Determines Decision-making Error in Rodents

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          Abstract

          Decision-making is a complex process that involves the integration and interpretation of sensory information to guide actions. The rodent motor cortex, which is generally involved in motor planning and execution, also plays a critical role in decision-making processes. In perceptual delayed-response tasks, the rodent motor cortex can represent sensory cues, as well as the decision of where to move. However, it remains unclear whether erroneous decisions arise from incorrect encoding of sensory information or improper utilization of the collected sensory information in the motor cortex. In this study, we analyzed the rodent anterior lateral motor cortex (ALM) while the mice performed perceptual delayed-response tasks. We divided population activities into sensory and choice signals to separately examine the encoding and utilization of sensory information. We found that the encoding of sensory information in the error trials was similar to that in the hit trials, whereas choice signals evolved differently between the error and hit trials. In error trials, choice signals displayed an offset in the opposite direction of instructed licking even before stimulus presentation, and this tendency gradually increased after stimulus onset, leading to incorrect licking. These findings suggest that decision errors are caused by biases in choice-related activities rather than by incorrect sensory encoding. Our study elaborates on the understanding of decision-making processes by providing neural substrates for erroneous decisions.

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          Most cited references25

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          Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings

          Measuring the dynamics of neural processing across time scales requires following the spiking of thousands of individual neurons over milliseconds and months. To address this need, we introduce the Neuropixels 2.0 probe together with newly designed analysis algorithms. The probe has more than 5000 sites and is miniaturized to facilitate chronic implants in small mammals and recording during unrestrained behavior. High-quality recordings over long time scales were reliably obtained in mice and rats in six laboratories. Improved site density and arrangement combined with newly created data processing methods enable automatic post hoc correction for brain movements, allowing recording from the same neurons for more than 2 months. These probes and algorithms enable stable recordings from thousands of sites during free behavior, even in small animals such as mice.
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            A motor cortex circuit for motor planning and movement.

            Activity in motor cortex predicts specific movements seconds before they occur, but how this preparatory activity relates to upcoming movements is obscure. We dissected the conversion of preparatory activity to movement within a structured motor cortex circuit. An anterior lateral region of the mouse cortex (a possible homologue of premotor cortex in primates) contains equal proportions of intermingled neurons predicting ipsi- or contralateral movements, yet unilateral inactivation of this cortical region during movement planning disrupts contralateral movements. Using cell-type-specific electrophysiology, cellular imaging and optogenetic perturbation, we show that layer 5 neurons projecting within the cortex have unbiased laterality. Activity with a contralateral population bias arises specifically in layer 5 neurons projecting to the brainstem, and only late during movement planning. These results reveal the transformation of distributed preparatory activity into movement commands within hierarchically organized cortical circuits.
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              Maintenance of persistent activity in a frontal thalamocortical loop

              Persistent neural activity maintains information bridging past and future events. Models of persistent activity often invoke reverberations within local cortical circuits, but long-range circuits could also contribute. Neurons in mouse anterior lateral motor cortex (ALM) show selective persistent activity that instructs future actions. ALM is connected bi-directionally with parts of the thalamus, including the ventral medial and ventral anterior-lateral nuclei. We recorded spikes from ALM and thalamus during tactile discrimination with a delayed directional response. Similar to ALM neurons, thalamic neurons exhibited selective persistent delay activity that predicted movement direction. Unilateral photoinhibition of delay activity in ALM or thalamus produced contralesional neglect. Photoinhibition of thalamus caused a short-latency and near total collapse of ALM activity. Similarly, photoinhibition of ALM diminished thalamic activity. Our results reveal thalamus as a circuit hub in motor preparation and suggest that persistent activity requires reciprocal excitation across multiple brain areas.
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                Author and article information

                Journal
                Exp Neurobiol
                Exp Neurobiol
                Experimental Neurobiology
                The Korean Society for Brain and Neural Sciences
                1226-2560
                2093-8144
                31 August 2023
                31 August 2023
                31 August 2023
                : 32
                : 4
                : 271-284
                Affiliations
                [1]Department of Biomedical Engineering, Ulsan National Institute of Science and Technology, Ulsan 44919, Korea
                Author notes
                [* ]To whom correspondence should be addressed. TEL: 82-52-217-2727, FAX: 82-52-217-2708, e-mail: spkim@ 123456unist.ac.kr
                Article
                en-32-4-271
                10.5607/en23020
                10569143
                37749928
                71c4548e-28ad-4d29-9d5b-ea041e738825
                Copyright © Experimental Neurobiology 2023

                This is an open-access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 7 July 2023
                : 23 August 2023
                : 30 August 2023
                Categories
                Original Article

                Neurosciences
                decision making,motor cortex,mice
                Neurosciences
                decision making, motor cortex, mice

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