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It is commonly agreed that a functional dissociation with respect to the internal vs external control of movements exists for several brain regions. This has, however, only been tested in relation to the timing and preparation of motor responses, but not to ongoing movement control. Using functional magnetic resonance imaging (fMRI), the present study addressed the neuroanatomical substrate of the internal–external control hypothesis by comparing regional brain activation for cyclical bimanual movements performed in the presence or absence of augmented visual feedback. Subjects performed a bimanual movement pattern, either with the help of on-line visual feedback of the movements (externally guided coordination) or with the eyes closed on the basis of an internal representation of the movement pattern (internally generated coordination). Visual control and baseline rest conditions were also added. Results showed a clear functional dissociation within the network involved in movement coordination. The hMT/V5+, the superior parietal cortex, the premotor cortex, the thalamus, and cerebellar lobule VI showed higher activation levels when movements were guided by visual feedback. Conversely, the basal ganglia, the supplementary motor area, cingulate motor cortex, the inferior parietal, frontal operculum, and cerebellar lobule IV-V/dentate nucleus showed higher involvement when movements were internally generated. Consequently, the present findings suggest the existence of distinct cortico-cortical and subcortico-cortical neural pathways for externally (augmented feedback) and internally guided cyclical bimanual movements. This provides a neurophysiological account for the beneficial effect of providing augmented visual feedback to optimize movements in normal and motor disordered patients.

Classical studies of mammalian movement control define a prominent role for the primary motor cortex. Investigating the mouse whisker system, we found an additional and equally direct pathway for cortical motor control driven by the primary somatosensory cortex. Whereas activity in primary motor cortex directly evokes exploratory whisker protraction, primary somatosensory cortex directly drives whisker retraction, providing a rapid negative feedback signal for sensorimotor integration. Motor control by sensory cortex suggests the need to reevaluate the functional organization of cortical maps.

Key Points The dorsomedial frontal cortex contains a cluster of areas that are designated the supplementary motor area (SMA), the supplementary eye field (SEF) and the pre-supplementary motor area (pre-SMA). The defining functional feature of the members of this supplementary motor complex (SMC) is a marked sensitivity to various aspects of action. The anatomical features of the SMC are not homogeneous: there is a gradient of morphological and connectional change where affinity with the prefrontal and primary motor cortices changes reciprocally in the rostro–caudal plane. More-rostral regions show greater kinship with the prefrontal cortex than with the primary motor cortex; for more-caudal regions the reverse is true. The SMC is also heterogeneous neurophysiologically. The subregions of the SMC show different patterns of effector predilection and exhibit relative differences in the preponderance of cells that are sensitive to more-complex aspects of action. Compared with primary motor areas, the SMC exhibits greater sensitivity to tasks in which action contingencies are broader in range and not unambiguously specified by the immediate external environment. This contrast is illustrated by differences in SMC activity between 'self-initiated' and 'externally triggered' actions, by movement sequences, by well-learnt and poorly learnt actions, and by switching between action possibilities. Damage to the SMC disrupts behaviour in complex ways, affecting not just the commission but also the omission of actions, and the effects are broadly reflective of the neurophysiological properties of the region. This plurality of functional responses has traditionally been taken as implying a plurality of neural functions, including implementing intentions, learning and performing temporally organized actions, switching between actions, and inhibiting unwanted actions. Traditional accounts of the role of the SMC in voluntary action assume a fundamentally discrete modular architecture, with different functions assigned to macroscopically defined and functionally homogeneous regions. Thus, one function could be assigned to the SMA (for example, performing sequences) and another could be assigned to the pre-SMA (for example, changing between sequences). To explain the full range of behaviours, these discrete units must be able to switch between different functions depending on task demands — a feature we term functional pleomorphism. Functional pleomorphism is conceptually problematic owing to the difficulty of explaining the process of switching between different neural functions. Moreover, a discrete modular architecture implies greater functional and structural homogeneity within functional modules than between them, a premise that is not supported by the empirical data. The differences across the region are better described by smoothly varying continuities than by any kind of discrete pattern, and they therefore need correspondingly smooth models of functional organization. The plurality of functions that has been assigned to the SMC is undercut by a single elemental confound: the conditional complexity of the underlying condition–action association. Framed in the terms of information theory, internal, sequential, new and otherwise-flexible actions require more information than externally triggered, non-sequential and well-learnt actions (which were previously considered to be matched in complexity). We suggest that gaining further insight into the role of the SMC requires a unified account of the region that is based on a faithful picture of the anatomical and neurophysiological features and a conceptually rigorous analysis of the models supposed to explain them. The supplementary motor complex has a role in regulating action, but whether each of its subregions has a distinct function is unclear. Husain and colleagues review the literature and discuss outstanding issues regarding the function of this complex. The supplementary motor complex consists of the supplementary motor area, the supplementary eye field and the pre-supplementary motor area. In recent years, these areas have come under increasing scrutiny from cognitive neuroscientists, motor physiologists and clinicians because they seem to be crucial for linking cognition to action. However, theories regarding their function vary widely. This Review brings together the data regarding the supplementary motor regions, highlighting outstanding issues and providing new perspectives for understanding their functions.

Motor control is an area of natural science exploring how the nervous system interacts with other body parts and the environment to produce purposeful, coordinated actions. A central problem of motor control—the problem of motor redundancy—was formulated by Nikolai Bernstein as the problem of elimination of redundant degrees-of-freedom. Traditionally, this problem has been addressed using optimization methods based on a variety of cost functions. This review draws attention to a body of recent findings suggesting that the problem has been formulated incorrectly. An alternative view has been suggested as the principle of abundance, which considers the apparently redundant degrees-of-freedom as useful and even vital for many aspects of motor behavior. Over the past 10 years, dozens of publications have provided support for this view based on the ideas of synergic control, computational apparatus of the uncontrolled manifold hypothesis, and the equilibrium-point (referent configuration) hypothesis. In particular, large amounts of “good variance”—variance in the space of elements that has no effect on the overall performance—have been documented across a variety of natural actions. “Good variance” helps an abundant system to deal with secondary tasks and unexpected perturbations; its amount shows adaptive modulation across a variety of conditions. These data support the view that there is no problem of motor redundancy; there is bliss of motor abundance.

Although inter-individual differences in performance are often considered to be 'noise', recent data show that they are linked to structural differences. Kanai and Rees argue that studying these links can help in understanding how structural variation influences the functional capacity of brain regions. Inter-individual variability in perception, thought and action is frequently treated as a source of 'noise' in scientific investigations of the neural mechanisms that underlie these processes, and discarded by averaging data from a group of participants. However, recent MRI studies in the human brain show that inter-individual variability in a wide range of basic and higher cognitive functions — including perception, motor control, memory, aspects of consciousness and the ability to introspect — can be predicted from the local structure of grey and white matter as assessed by voxel-based morphometry or diffusion tensor imaging. We propose that inter-individual differences can be used as a source of information to link human behaviour and cognition to brain anatomy.

Key Points The mirror mechanism is the mechanism that unifies perception and action, transforming sensory representations of the behaviour of others into motor representations of the same behaviour in the brain of the observer. The parieto-frontal mirror circuit is the most studied of the circuits endowed with the mirror mechanism. Yet, there is still controversy about its role in social cognition and its contribution to understanding the actions and intentions of other individuals. Recent findings show that the parieto-frontal mirror circuit in monkeys encodes the goal of the observed motor acts. In humans, there is evidence that the same circuit encodes the goal of the observed motor act and its individual movements. The analysis of the properties of parieto-frontal mirror neurons shows that these neurons can encode the observed motor acts with a high degree of generality. None of the visual areas seems to have such a generality. This indicates that the parieto-frontal mirror circuit has a crucial role in understanding the actions of others. The mirror mechanism is also involved in understanding the intentions of others. This capacity is mediated by the organization of the parieto-frontal mirror circuit in chains of neurons, in which each neuron encodes a specific motor act. This organization is present in both monkeys and humans, and recent studies have shown that it is impaired in children with autism. Although the intentions of others might be understood in various ways, the mirror-based intention understanding is the only way that allows an individual to understand the actions of others 'from the inside' and provides the observer with a first-person grasp of another individual's motor goals and intentions. The putative role of the parieto-frontal mirror circuit in action understanding is hotly debated. Reviewing studies in monkeys and humans, Rizzolatti and Sinigaglia describe what parieto-frontal mirror neurons encode, discuss the cognitive functions this circuit might support and address outstanding issues of controversy. The parieto-frontal cortical circuit that is active during action observation is the circuit with mirror properties that has been most extensively studied. Yet, there remains controversy on its role in social cognition and its contribution to understanding the actions and intentions of other individuals. Recent studies in monkeys and humans have shed light on what the parieto-frontal cortical circuit encodes and its possible functional relevance for cognition. We conclude that, although there are several mechanisms through which one can understand the behaviour of other individuals, the parieto-frontal mechanism is the only one that allows an individual to understand the action of others 'from the inside' and gives the observer a first-person grasp of the motor goals and intentions of other individuals.

The anterior insular cortex is activated by a wide range of conditions and behaviours that go beyond interoception. In a provocative Perspective, Bud Craig proposes that the anterior insula has a fundamental role in human awareness. The anterior insular cortex (AIC) is implicated in a wide range of conditions and behaviours, from bowel distension and orgasm, to cigarette craving and maternal love, to decision making and sudden insight. Its function in the re-representation of interoception offers one possible basis for its involvement in all subjective feelings. New findings suggest a fundamental role for the AIC (and the von Economo neurons it contains) in awareness, and thus it needs to be considered as a potential neural correlate of consciousness.

Key Points Direction-selective retinal ganglions cells (DSGCs) consist of several distinct types that branch at different levels in the inner retina. Most types are comprised of multiple subtypes, each of which responds to image motion in a different preferred direction. Recent studies have identified specific molecular markers that are expressed either endogenously or transgenically by particular subtypes of DSGC. In most cases, the key player in the generation of direction selectivity in the retina is the starburst amacrine cell (SAC), which is a morphologically symmetrical interneuron that contains both GABA and acetylcholine (ACh). The release of GABA from individual distal dendrites of SACs is itself direction selective, owing to the sequential activation of excitatory inputs along the dendrite together with intrinsic nonlinearities in the SAC; inhibitory interactions between overlapping SACs also seem to have a role. The directional output from individual dendrites is preserved because dendrites on different sides of the SAC make selective inhibitory synapses on different subtypes of DSGCs, thus establishing their preferred direction. The centrifugal separation of input and output synapses along the SAC dendrites provides the fundamental spatial asymmetry that underlies the generation of direction selectivity in the retina. The asymmetric GABAergic inhibition from SACs interacts with symmetric cholinergic excitation from SACs and glutamatergic excitation from bipolar cells within local regions of the DSGC's dendritic tree. The summed inputs within each of these functional subunits are locally thresholded, producing dendritic spikes that propagate to the soma independently of the activity in other subunits. The development of the different subtypes of DSGCs and their selective connectivity with the SACs seems to be mainly governed by intrinsic mechanisms, with visual stimulation and spontaneous neuronal activity playing negligible roles. Processing within neural circuits in the retina extracts information about the direction of motion of images projected onto the retina. Vaney and colleagues describe the cellular components of this circuitry and outline our current understanding of the mechanisms that are involved in generating direction-selective responses in the retina. Visual information is processed in the retina to a remarkable degree before it is transmitted to higher visual centres. Several types of retinal ganglion cells (the output neurons of the retina) respond preferentially to image motion in a particular direction, and each type of direction-selective ganglion cell (DSGC) is comprised of multiple subtypes with different preferred directions. The direction selectivity of the cells is generated by diverse mechanisms operating within microcircuits that rely on independent neuronal processing in individual dendrites of both the DSGCs and the presynaptic neurons that innervate them.

In vivo effects of transcranial direct current stimulation (tDCS) have attracted much attention nowadays as this area of research spreads to both the motor and cognitive domains. The common assumption is that the anode electrode causes an enhancement of cortical excitability during stimulation, which then lasts for a few minutes thereafter, while the cathode electrode generates the opposite effect, i.e., anodal-excitation and cathodal-inhibition effects (AeCi). Yet, this dual-polarity effect has not been observed in all tDCS studies. Here, we conducted a meta-analytical review aimed to investigate the homogeneity/heterogeneity of the effect sizes of the AeCi dichotomy in both motor and cognitive functions. The AeCi effect was found to occur quite commonly with motor investigations and rarely in cognitive studies. When the anode electrode is applied over a non-motor area, in most cases, it will cause an excitation as measured by a relevant cognitive or perceptual task; however, the cathode electrode rarely causes an inhibition. We found homogeneity in motor studies and heterogeneity in cognitive studies with the electrode’s polarity serving as a moderator that can explain the source of heterogeneity in cognitive studies. The lack of inhibitory cathodal effects might reflect compensation processes as cognitive functions are typically supported by rich brain networks. Further insights as to the polarity and domain interaction are offered, including subdivision to different classes of cognitive functions according to their likelihood of being affected by stimulation.

In an auditory frequency discrimination task in rats, channelrhodopsin-2-mediated stimulation of corticostriatal neurons biases decisions in the direction predicted by the frequency tuning of the stimulated neurons, whereas archaerhodopsin-3-mediated inactivation biases decisions in the opposite direction. Sound decisions in the auditory cortex Many studies have established how sounds are represented in the auditory cortex, but the processes by which that coded information is transformed into action are less well understood. Petr Znamenskiy and Anthony Zador study one output of auditory cortex — the projections to the striatum — and explore the consequences of changing the activity of these neurons on rats' perceptions in an auditory task. Optogenetically manipulating neuronal activity biased decisions in a manner consistent with the properties of the stimulated neurons, implicating corticostriatal activity in sensorimotor transformations. As cortical areas corresponding to all sensory modalities project to the striatum, this work also has implications beyond the auditory system. The neural pathways by which information about the acoustic world reaches the auditory cortex are well characterized, but how auditory representations are transformed into motor commands is not known. Here we use a perceptual decision-making task in rats to study this transformation. We demonstrate the role of corticostriatal projection neurons in auditory decisions by manipulating the activity of these neurons in rats performing an auditory frequency-discrimination task. Targeted channelrhodopsin-2 (ChR2) 1 , 2 -mediated stimulation of corticostriatal neurons during the task biased decisions in the direction predicted by the frequency tuning of the stimulated neurons, whereas archaerhodopsin-3 (Arch) 3 -mediated inactivation biased decisions in the opposite direction. Striatal projections are widespread in cortex and may provide a general mechanism for the control of motor decisions by sensory cortex.