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      A motor cortex circuit for motor planning and movement

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          Abstract

          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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          Most cited references43

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          ReaChR: A red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation

          Channelrhodopsins are used to optogenetically depolarize neurons. We engineered a variant of channelrhodopsin, denoted Re d- a ctivatable Ch annel r hodopsin (ReaChR), that is optimally excited with orange to red light (λ ~ 590 to 630 nm) and offers improved membrane trafficking, higher photocurrents, and faster kinetics compared with existing red-shifted channelrhodopsins. Red light is more weakly scattered by tissue and absorbed less by blood than the blue to green wavelengths required by other channelrhodopsin variants. ReaChR expressed in vibrissa motor cortex was used to drive spiking and vibrissa motion in awake mice when excited with red light through intact skull. Precise vibrissa movements were evoked by expressing ReaChR in the facial motor nucleus in the brainstem and illuminating with red light through the external auditory canal. Thus, ReaChR enables transcranial optical activation of neurons in deep brain structures without the need to surgically thin the skull, form a transcranial window, or implant optical fibers.
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            What is the Bereitschaftspotential?

            Since discovery of the slow negative electroencephalographic (EEG) activity preceding self-initiated movement by Kornhuber and Deecke [Kornhuber HH, Deecke L. Hirnpotentialänderungen bei Willkurbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflugers Archiv 1965;284:1-17], various source localization techniques in normal subjects and epicortical recording in epilepsy patients have disclosed the generator mechanisms of each identifiable component of movement-related cortical potentials (MRCPs) to some extent. The initial slow segment of BP, called 'early BP' in this article, begins about 2 s before the movement onset in the pre-supplementary motor area (pre-SMA) with no site-specificity and in the SMA proper according to the somatotopic organization, and shortly thereafter in the lateral premotor cortex bilaterally with relatively clear somatotopy. About 400 ms before the movement onset, the steeper negative slope, called 'late BP' in this article (also referred to as NS'), occurs in the contralateral primary motor cortex (M1) and lateral premotor cortex with precise somatotopy. These two phases of BP are differentially influenced by various factors, especially by complexity of the movement which enhances only the late BP. Event-related desynchronization (ERD) of beta frequency EEG band before self-initiated movements shows a different temporospatial pattern from that of the BP, suggesting different neuronal mechanisms for the two. BP has been applied for investigating pathophysiology of various movement disorders. Volitional motor inhibition or muscle relaxation is preceded by BP quite similar to that preceding voluntary muscle contraction. Since BP of typical waveforms and temporospatial pattern does not occur before organic involuntary movements, BP is used for detecting the participation of the 'voluntary motor system' in the generation of apparently involuntary movements in patients with psychogenic movement disorders. In view of Libet et al.'s report [Libet B, Gleason CA, Wright EW, Pearl DK. Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 1983;106:623-642] that the awareness of intention to move occurred much later than the onset of BP, the early BP might reflect, physiologically, slowly increasing cortical excitability and, behaviorally, subconscious readiness for the forthcoming movement. Whether the late BP reflects conscious preparation for intended movement or not remains to be clarified.
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              Cortical control of arm movements: a dynamical systems perspective.

              Our ability to move is central to everyday life. Investigating the neural control of movement in general, and the cortical control of volitional arm movements in particular, has been a major research focus in recent decades. Studies have involved primarily either attempts to account for single-neuron responses in terms of tuning for movement parameters or attempts to decode movement parameters from populations of tuned neurons. Even though this focus on encoding and decoding has led to many seminal advances, it has not produced an agreed-upon conceptual framework. Interest in understanding the underlying neural dynamics has recently increased, leading to questions such as how does the current population response determine the future population response, and to what purpose? We review how a dynamical systems perspective may help us understand why neural activity evolves the way it does, how neural activity relates to movement parameters, and how a unified conceptual framework may result.
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                Author and article information

                Journal
                Nature
                Nature
                Springer Science and Business Media LLC
                0028-0836
                1476-4687
                March 2015
                February 25 2015
                March 2015
                : 519
                : 7541
                : 51-56
                Article
                10.1038/nature14178
                25731172
                e759b172-6d8a-4f6b-b1bd-2868dec0f936
                © 2015

                http://www.springer.com/tdm

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