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Evidence has demonstrated that athletes exhibit superior cognitive performance associated with executive control. In the oculomotor system, this function has been examined using the interleaved pro‐saccade and anti‐saccade task (IPAST), wherein participants, prior to target appearance, are instructed to either automatically look at the peripheral target (pro‐saccade) or suppress the automatic response and voluntarily look in the opposite direction (anti‐saccade). While the IPAST has provided much insight into sensorimotor and inhibitory processing, it has yet to be performed in athletes. Moreover, limited research has examined saccade metrics in athletes. Here, we examined saccade latency and movement kinematics in the IPAST among athletes (N = 40) and nonathletes (NON) (N = 40). Higher direction error rates were obtained in the anti‐saccade compared to the pro‐saccade condition, with no differences between athletes and NON noted. Significantly faster saccade latencies were observed in athletes compared to NON in both conditions, in addition to faster pro‐saccades compared to anti‐saccades. Furthermore, athletes showed significantly higher frequencies and faster latencies of express saccades compared to NON in correct pro‐saccades. Additionally, athletes exhibited significantly faster latencies of express saccades compared to NON in erroneous anti‐saccades. Differences in saccade metrics between athletes and NON were not seen. Overall, these findings demonstrate that athletes display altered saccade performance likely associated with sensorimotor and preparatory processing, highlighting the potential of using IPAST to objectively investigate sensorimotor and cognitive functions in athletes. [ABSTRACT FROM AUTHOR]

A learned sensory-motor behavior engages multiple brain regions, including the neocortex and the basal ganglia. How a target stimulus is detected by these regions and converted to a motor response remains poorly understood. Here, we performed electrophysiological recordings and pharmacological inactivations of whisker motor cortex and dorsolateral striatum to determine the representations within, and functions of, each region during performance in a selective whisker detection task in male and female mice. From the recording experiments, we observed robust, lateralized sensory responses in both structures. We also observed bilateral choice probability and preresponse activity in both structures, with these features emerging earlier in whisker motor cortex than dorsolateral striatum. These findings establish both whisker motor cortex and dorsolateral striatum as potential contributors to the sensory-to-motor (sensorimotor) transformation. We performed pharmacological inactivation studies to determine the necessity of these brain regions for this task. We found that suppressing the dorsolateral striatum severely disrupts responding to task-relevant stimuli, without disrupting the ability to respond, whereas suppressing whisker motor cortex resulted in more subtle changes in sensory detection and response criterion. Together these data support the dorsolateral striatum as an essential node in the sensorimotor transformation of this whisker detection task.SIGNIFICANCE STATEMENT Selecting an item in a grocery store, hailing a cab - these daily practices require us to transform sensory stimuli into motor responses. Many decades of previous research have studied goal-directed sensory-to-motor transformations within various brain structures, including the neocortex and the basal ganglia. Yet, our understanding of how these regions coordinate to perform sensory-to-motor transformations is limited because these brain structures are often studied by different researchers and through different behavioral tasks. Here, we record and perturb specific regions of the neocortex and the basal ganglia and compare their contributions during performance of a goal-directed somatosensory detection task. We find notable differences in the activities and functions of these regions, which suggests specific contributions to the sensory-to-motor transformation process.

The acquisition of new motor skills from scratch, also known as de novo learning, is an essential aspect of motor development. In de novo learning, the ability to generalize skills acquired under one condition to others is crucial because of the inherently limited range of motor experiences available for learning. However, the presence of generalization in de novo learning and its influencing factors remain unclear. This study aimed to elucidate the generalization of de novo motor learning by examining the motor exploration process, which is the accumulation of motor experiences. To this end, we manipulated the exploration process during practice by changing the target shape using either a small circular target or a bar-shaped target. Our findings demonstrated that the amount of learning during practice was generalized across different conditions. Furthermore, the extent of generalization is influenced by movement variability in the control space, which is irrelevant to the task, rather than the target shapes themselves. These results confirmed the occurrence of generalization in de novo learning and suggest that the exploration process within the control space plays a significant role in facilitating this generalization.

During natural viewing, we often recognize multiple objects, detect their motion, and select one object as the target to track. It remains to be determined how such behavior is guided by the integration of visual form and motion perception. To address this, we studied how monkeys made a choice to track moving targets with different forms by smooth pursuit eye movements in a two-target task. We found that pursuit responses were biased toward the motion direction of a target with a hole. By computing the relative weighting, we found that the target with a hole exhibited a larger weight for vector computation. The global hole feature dominated other form properties. This dominance failed to account for changes in pursuit responses to a target with different forms moving singly. These findings suggest that the integration of visual form and motion perception can reshape the competition in sensorimotor networks to guide behavioral selection. [ABSTRACT FROM AUTHOR]

Predatory hunting is an important type of innate behavior evolutionarily conserved across the animal kingdom. It is typically composed of a set of sequential actions, including prey search, pursuit, attack, and consumption. This behavior is subject to control by the nervous system. Early studies used toads as a model to probe the neuroethology of hunting, which led to the proposal of a sensory-triggered release mechanism for hunting actions. More recent studies have used genetically-trackable zebrafish and rodents and have made breakthrough discoveries in the neuroethology and neurocircuits underlying this behavior. Here, we review the sophisticated neurocircuitry involved in hunting and summarize the detailed mechanism for the circuitry to encode various aspects of hunting neuroethology, including sensory processing, sensorimotor transformation, motivation, and sequential encoding of hunting actions. We also discuss the overlapping brain circuits for hunting and feeding and point out the limitations of current studies. We propose that hunting is an ideal behavioral paradigm in which to study the neuroethology of motivated behaviors, which may shed new light on epidemic disorders, including binge-eating, obesity, and obsessive-compulsive disorders. [ABSTRACT FROM AUTHOR]

Recent studies in mice reveal widespread cortical signals during task performance; however, the various task-related and task-independent processes underlying this activity are incompletely understood. Here, we recorded wide-field neural activity, as revealed by GCaMP6s, from dorsal cortex while simultaneously monitoring orofacial movements, walking, and arousal (pupil diameter) of head-fixed mice performing a Go/NoGo visual detection task and examined the ability of task performance and spontaneous or task-related movements to predict cortical activity. A linear model was able to explain a significant fraction (33-55% of variance) of widefield dorsal cortical activity, with the largest factors being movements (facial, walk, eye), response choice (hit, miss, false alarm), and arousal and indicate that a significant fraction of trial-to-trial variability arises from both spontaneous and task-related changes in state (e.g., movements, arousal). Importantly, secondary motor cortex was highly correlated with lick rate, critical for optimal task performance (high d'), and was the first region to significantly predict the lick response on target trials. These findings suggest that secondary motor cortex is critically involved in the decision and performance of learned movements and indicate that a significant fraction of trial-to-trial variation in cortical activity results from spontaneous and task-related movements and variations in behavioral/arousal state.

Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

Flexibly selecting appropriate actions in response to complex, ever-changing environments requires both cortical and subcortical regions, which are typically described as participating in a strict hierarchy. In this traditional view, highly specialized subcortical circuits allow for efficient responses to salient stimuli, at the cost of adaptability and context specificity, which are attributed to the neocortex. Their interactions are often described as the cortex providing top-down command signals for subcortical structures to implement; however, as available technologies develop, studies increasingly demonstrate that behavior is represented by brainwide activity and that even subcortical structures contain early signals of choice, suggesting that behavioral functions emerge as a result of different regions interacting as truly collaborative networks. In this review, we discuss the field's evolving understanding of how cortical and subcortical regions in placental mammals interact cooperatively, not only via top-down cortical-subcortical inputs but through bottom-up interactions, especially via the thalamus. We describe our current understanding of the circuitry of both the cortex and two exemplar subcortical structures, the superior colliculus and striatum, to identify which information is prioritized by which regions. We then describe the functional circuits these regions form with one another, and the thalamus, to create parallel loops and complex networks for brainwide information flow. Finally, we challenge the classic view that functional modules are contained within specific brain regions; instead, we propose that certain regions prioritize specific types of information over others, but the subnetworks they form, defined by their anatomical connections and functional dynamics, are the basis of true specialization. [ABSTRACT FROM AUTHOR]

To generate a hand-specific reach plan, the brain must integrate hand-specific signals with the desired movement strategy. Although various neurophysiology/imaging studies have investigated hand-target interactions in simple reach-to-target tasks, the whole brain timing and distribution of this process remain unclear, especially for more complex, instruction-dependent motor strategies. Previously, we showed that a pro/anti pointing instruction influences magnetoencephalographic (MEG) signals in frontal cortex that then propagate recurrently through parietal cortex (Blohm G, Alikhanian H, Gaetz W, Goltz HC, DeSouza JF, Cheyne DO, Crawford JD. NeuroImage 197: 306-319, 2019). Here, we contrasted left versus right hand pointing in the same task to investigate 1) which cortical regions of interest show hand specificity and 2) which of those areas interact with the instructed motor plan. Eight bilateral areas, the parietooccipital junction (POJ), superior parietooccipital cortex (SPOC), supramarginal gyrus (SMG), medial/anterior interparietal sulcus (mIPS/aIPS), primary somatosensory/motor cortex (S1/M1), and dorsal premotor cortex (PMd), showed hand-specific changes in beta band power, with four of these (M1, S1, SMG, aIPS) showing robust activation before movement onset. M1, SMG, SPOC, and aIPS showed significant interactions between contralateral hand specificity and the instructed motor plan but not with bottom-up target signals. Separate hand/motor signals emerged relatively early and lasted through execution, whereas hand-motor interactions only occurred close to movement onset. Taken together with our previous results, these findings show that instruction-dependent motor plans emerge in frontal cortex and interact recurrently with handspecific parietofrontal signals before movement onset to produce hand-specific motor behaviors. [ABSTRACT FROM AUTHOR]

The posterior "tail" region of the striatum receives dense innervation from sensory brain regions and is important for behaviors that require sensorimotor integration. The output neurons of the striatum, D1 and D2 striatal projection neurons (SPNs), which make up the direct and indirect pathways, are thought to play distinct functional roles, although it remains unclear if these neurons show cell-type-specific differences in their response to sensory stimuli. Here, we examine the strength of synaptic inputs onto D1 and D2 SPNs following the stimulation of upstream auditory pathways. We report that auditory-evoked depolarizations onto D1 SPN responses are stronger and faster. This is due to differences in feedforward inhibition, with fast-spiking interneurons forming stronger synapses onto D2 SPNs. Our results support a model in which differences in feedforward inhibition enable the preferential recruitment of D1 SPNs by auditory stimuli, positioning the direct pathway to initiate sound-driven actions., Competing Interests: Declaration of interests The authors have no interests to declare., (Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.)

Skilled forelimb control is essential for daily living, yet our understanding of its neural mechanisms, although extensive, remains incomplete. Here, we present evidence that the superior colliculus (SC), a major midbrain structure, is necessary for accurate forelimb reaching in mice. We found that neurons in the lateral SC are active during goal-directed reaching, and by employing chemogenetic and phase-specific optogenetic silencing of these neurons, we show that the SC causally facilitates reach accuracy. Anatomical studies identified the deep cerebellar nuclei and substantia nigra pars reticulata as sources of inputs to the SC, while functional studies revealed a role for nigrotectal, but not cerebellotectal, neurons in controlling reach endpoints. Silencing the nigrotectal pathway caused paw deviations opposite to those seen with SC silencing, emphasizing the coordinated role of the substantia nigra and SC in regulating optimal reaching. Together, these findings establish the SC as a crucial regulator of skilled forelimb control., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)

Goal-directed actions require transforming sensory information into motor plans defined across multiple parameters and reference frames. Substantial evidence supports the encoding of target direction in gaze- and body-centered coordinates within parietal and premotor regions. However, how the brain encodes the equally critical parameter of target distance remains less understood. Here, using Bayesian pattern component modeling of fMRI data during a delayed reach-to-target task, we dissociated the neural encoding of both target direction and the relative distances between target, gaze, and hand at early and late stages of motor planning. This approach revealed independent representations of direction and distance along the human dorsomedial reach pathway. During early planning, most premotor and superior parietal areas encoded a target's distance in single or multiple reference frames and encoded its direction. In contrast, distance encoding was magnified in gaze- and body-centric reference frames during late planning. These results emphasize a flexible and efficient human central nervous system that achieves goals by remapping sensory information related to multiple parameters, such as distance and direction, in the same brain areas., Competing Interests: The authors declare no competing financial interests., (Copyright © 2024 Caceres et al.)

The COVID-19 pandemic has accelerated interest in virtual reality (VR) for education, entertainment, telerehabilitation, and skills training. As the frequency and duration of VR engagement increases—the number of people in the United States using VR at least once per month is forecasted to exceed 95 million—it is critical to understand how VR engagement influences brain and behavior. Here, we evaluate neurophysiological effects of sensory conflicts induced by VR engagement and posit an intriguing hypothesis: the brain processes VR as a unique “context” leading to the formation and maintenance of independent sensorimotor representations. We discuss known VR-induced sensorimotor adaptations to illustrate how VR might manifest as a context for learning and how technological and human factors might mediate the context-dependency of sensorimotor representations learned in VR.

The coleoid cephalopods (cuttlefish, octopus, and squid) are a group of soft-bodied mollusks that exhibit a wealth of complex behaviors, including dynamic camouflage, object mimicry, skin-based visual communication, and dynamic body patterns during sleep. Many of these behaviors are visually driven and engage the animals' color changing skin, a pixelated display that is directly controlled by neurons projecting from the brain. Thus, cephalopod skin provides a direct readout of neural activity in the brain. During camouflage, cephalopods recreate on their skin an approximation of what they see, providing a window into perceptual processes in the brain. Additionally, cephalopods communicate their internal state during social encounters using innate skin patterns, and create waves of pigmentation on their skin during periods of arousal. Thus, by leveraging the visual displays of cephalopods, we can gain insight into how the external world is represented in the brain and how this representation is transformed into a recapitulation of the world on the skin. Here, we describe the rich skin behaviors of the coleoid cephalopods, what is known about cephalopod neuroanatomy, and how advancements in gene editing, machine learning, optical imaging, and electrophysiological tools may provide an opportunity to explore the neural bases of these fascinating behaviors. • Cephalopods control their skin color, pattern, and texture using their brain. • Dynamic skin patterning is used for camouflage and social behaviors. • Camouflage patterns provide a readout of the animal's perception of the world. • Social skin patterns are an external manifestation of internal state. [ABSTRACT FROM AUTHOR]

Sensorimotor transformation, a process that converts sensory stimuli into motor actions, is critical for the brain to initiate behaviors. Although the circuitry involved in sensorimotor transformation has been well delineated, the molecular logic behind this process remains poorly understood. Here, we performed high-throughput and circuit-specific single-cell transcriptomic analyses of neurons in the superior colliculus (SC), a midbrain structure implicated in early sensorimotor transformation. We found that SC neurons in distinct laminae expressed discrete marker genes. Of particular interest, Cbln2 and Pitx2 were key markers that define glutamatergic projection neurons in the optic nerve (Op) and intermediate gray (InG) layers, respectively. The Cbln2+ neurons responded to visual stimuli mimicking cruising predators, while the Pitx2+ neurons encoded prey-derived vibrissal tactile cues. By forming distinct input and output connections with other brain areas, these neuronal subtypes independently mediated behaviors of predator avoidance and prey capture. Our results reveal that, in the midbrain, sensorimotor transformation for different behaviors may be performed by separate circuit modules that are molecularly defined by distinct transcriptomic codes.

The brain processes sensory information in a context- and learning-dependent manner for adaptive behavior. Through reward-based learning, relevant sensory stimuli can become linked to execution of specific actions associated with positive outcomes. The neuronal circuits involved in such goal-directed sensory-to-motor transformations remain to be precisely determined. Studying simple learned sensorimotor transformations in head-restrained mice offers the opportunity for detailed measurements of cellular activity during task performance. Here, we trained mice to lick a reward spout in response to a whisker deflection and an auditory tone. Through two-photon calcium imaging of retrogradely labeled neurons, we found that neurons located in primary whisker somatosensory barrel cortex projecting to secondary whisker somatosensory cortex had larger calcium signals than neighboring neurons projecting to primary whisker motor cortex in response to whisker deflection and auditory stimulation, as well as before spontaneous licking. Longitudinal imaging of the same neurons revealed that these projection-specific responses were relatively stable across 3 days. In addition, the activity of neurons projecting to secondary whisker somatosensory cortex was more highly correlated than for neurons projecting to primary whisker motor cortex. The large and correlated activity of neurons projecting to secondary whisker somatosensory cortex might enhance the pathway-specific signaling of important sensory information contributing to task execution. Our data support the hypothesis that communication between primary and secondary somatosensory cortex might be an early critical step in whisker sensory perception. More generally, our data suggest the importance of investigating projection-specific neuronal activity in distinct populations of intermingled excitatory neocortical neurons during task performance. [ABSTRACT FROM AUTHOR]

Background. Previous studies have shown that brain response to a written word depends on the task: whether the word is a target in a version of lexical decision task or should be read silently. Although this effect has been interpreted as an evidence for an interaction between word recognition processes and task demands, it also may be caused by greater attention allocation to the target word. Objective. We aimed to examine the task effect on brain response evoked by non- target written words. Design. Using MEG and magnetic source imaging, we compared spatial-temporal pattern of brain response elicited by a noun cue when it was read silently either without additional task (SR) or with a requirement to produce an associated verb (VG). Results.The task demands penetrated into early (200-300 ms) and late (500-800 ms) stages of a word processing by enhancing brain response under VG versus SR condition. The cortical sources of the early response were localized to bilateral inferior occipitotemporal and anterior temporal cortex suggesting that more demanding VG task required elaborated lexical-semantic analysis. The late effect was observed in the associative auditory areas in middle and superior temporal gyri and in motor representation of articulators. Our results suggest that a remote goal plays a pivotal role in enhanced recruitment of cortical structures underlying orthographic, semantic and sensorimotor dimensions of written word perception from the early processing stages. Surprisingly, we found that to fulfil a more challenging goal the brain progressively engaged resources of the right hemisphere throughout all stages of silent reading. Conclusion. Our study demonstrates that a deeper processing of linguistic input amplifies activation of brain areas involved in integration of speech perception and production. This is consistent with theories that emphasize the role of sensorimotor integration in speech understanding.

Sensation and action are necessarily coupled during stimulus perception – while tasting, for instance, perception happens while an animal decides to expel or swallow the substance in the mouth (the former via a behavior known as ‘gaping’). Taste responses in the rodent gustatory cortex (GC) span this sensorimotor divide, progressing through firing-rate epochs that culminate in the emergence of action-related firing. Population analyses reveal this emergence to be a sudden, coherent and variably-timed ensemble transition that reliably precedes gaping onset by 0.2–0.3s. Here, we tested whether this transition drives gaping, by delivering 0.5s GC perturbations in tasting trials. Perturbations significantly delayed gaping, but only when they preceded the action-related transition - thus, the same perturbation impacted behavior or not, depending on the transition latency in that particular trial. Our results suggest a distributed attractor network model of taste processing, and a dynamical role for cortex in driving motor behavior.

Abstract Prolonged musical training induces important audio-visuo-motor plastic processes. However, little is known about how the musicians' brain resolves multimodal conflicts while preparing for musical action. We run an electroencephalographic (EEG) investigation on how visual processing for action (score reading) is affected by preceding task-irrelevant piano sounds, usually associated to the same or to a different action. Presentation of an incongruent sound, 100 msec before a musical score with one single note, reduces Event-Related Potentials (ERPs) associated to score reading (N170) localised in the right temporo-parietal junction, as well as ERPs associated to conflict strength (N2) localised in the anterior cingulate cortex, superior and inferior right frontal cortex. These results suggest that listening to task-irrelevant auditory action effects (musical notes) interferes with both higher-order visual and frontal conflict monitoring processes. We conclude that, in the musicians' brain, the automatic translation of musical sounds into motor plans, spread its effects to visually specific processing as well as strategic and amodal action monitoring mechanisms. [ABSTRACT FROM AUTHOR]

Goal-directed behaviors involve coordinated activity in many cortical areas, but whether the encoding of task variables is distributed across areas or is more specifically represented in distinct areas remains unclear. Here, we compared representations of sensory, motor, and decision information in the whisker primary somatosensory cortex, medial prefrontal cortex, and tongue-jaw primary motor cortex in mice trained to lick in response to a whisker stimulus with mice that were not taught this association. Irrespective of learning, properties of the sensory stimulus were best encoded in the sensory cortex, whereas fine movement kinematics were best represented in the motor cortex. However, movement initiation and the decision to lick in response to the whisker stimulus were represented in all three areas, with decision neurons in the medial prefrontal cortex being more selective, showing minimal sensory responses in miss trials and motor responses during spontaneous licks. Our results reconcile previous studies indicating highly specific vs. highly distributed sensorimotor processing. [Display omitted] • Highly distributed neocortical activity as mice lick in response to whisker stimuli • Task-independent encoding of whisker stimulus properties only in sensory cortex • Task-independent coding of precise tongue movement kinematics only in motor cortex • Learned highly selective representation of decision in prefrontal cortex Combining high-density extracellular electrophysiological recordings with high-speed videography of orofacial movements of mice performing a psychometric whisker sensory detection task reported by licking, Oryshchuk et al. found overall highly distributed task-related neuronal activity, but sensory, motor, and decision information were most selectively represented, respectively, in sensory, motor, and prefrontal cortices. [ABSTRACT FROM AUTHOR]

Sensory navigation results from coordinated transitions between distinct behavioral programs. During chemotaxis in the Drosophila melanogaster larva, the detection of positive odor gradients extends runs while negative gradients promote stops and turns. This algorithm represents a foundation for the control of sensory navigation across phyla. In the present work, we identified an olfactory descending neuron, PDM-DN, which plays a pivotal role in the organization of stops and turns in response to the detection of graded changes in odor concentrations. Artificial activation of this descending neuron induces deterministic stops followed by the initiation of turning maneuvers through head casts. Using electron microscopy, we reconstructed the main pathway that connects the PDM-DN neuron to the peripheral olfactory system and to the pre-motor circuit responsible for the actuation of forward peristalsis. Our results set the stage for a detailed mechanistic analysis of the sensorimotor conversion of graded olfactory inputs into action selection to perform goal-oriented navigation.

The mouse superior colliculus (SC) is a laminar midbrain structure involved in processing and transforming multimodal sensory stimuli into ethologically relevant behaviors such as escape, defense, and orienting movements. The SC is unique in that the sensory (visual, auditory, and somatosensory) and motor maps are overlaid. In the mouse, the SC receives inputs from more retinal ganglion cells than any other visual area. This makes the mouse SC an ideal model system for understanding how visual signals processed by retinal circuits are used to mediate visually guided behaviors. This Perspective provides an overview of the current understanding of visual motor transformations operated by the mouse SC and discusses the challenges to be overcome when investigating the input–output relationships in single collicular cell types.

Over the last half century, work with flies, bees, and moths have revealed a number of visual guidance strategies for controlling different aspects of flight. Some algorithms, such as the use of pattern velocity in forward flight, are employed by all insects studied so far, and are used to control multiple flight tasks such as regulation of speed, measurement of distance, and positioning through narrow passages. Although much attention has been devoted to long-range navigation and homing in birds, until recently, very little was known about how birds control flight in a moment-to-moment fashion. A bird that flies rapidly through dense foliage to land on a branch—as birds often do—engages in a veritable three-dimensional slalom, in which it has to continually dodge branches and leaves, and find, and possibly even plan a collision-free path to the goal in real time. Each mode of flight from take-off to goal could potentially involve a different visual guidance algorithm. Here, we briefly review strategies for visual guidance of flight in insects, synthesize recent work from short-range visual guidance in birds, and offer a general comparison between the two groups of organisms.

The mouse superior colliculus (SC) is a laminar midbrain structure involved in processing and transforming multimodal sensory stimuli into ethologically relevant behaviors such as escape, defense, and orienting movements. The SC is unique in that the sensory (visual, auditory, and somatosensory) and motor maps are overlaid. In the mouse, the SC receives inputs from more retinal ganglion cells than any other visual area. This makes the mouse SC an ideal model system for understanding how visual signals processed by retinal circuits are used to mediate visually guided behaviors. This Perspective provides an overview of the current understanding of visual motor transformations operated by the mouse SC and discusses the challenges to be overcome when investigating the input–output relationships in single collicular cell types. [ABSTRACT FROM AUTHOR]

When a saccadic eye movement is made toward a visual stimulus, the variability in accompanying primary visual cortex (V1) activity is related to saccade latency in both humans and simians. To understand the nature of this relationship, we examined the functional link between V1 activity and the initiation of visually guided saccades during the gap saccade task, in which a brief temporal gap is inserted between the turning off of a fixation stimulus and the appearance of a saccadic target. The insertion of such a gap robustly reduces saccade latency and facilitates the occurrence of extremely short-latency (express) saccades. Here we recorded single-cell activity from macaque V1 while monkeys performed the gap saccade task. In parallel with the gap effect on saccade latency the neural latency (time of first spike) of V1 response elicited by the saccade target became shorter, and the firing rate increased as the gap duration increased. Similarly, neural latency was shorter and firing rate was higher before express saccades relative to regular-latency saccades. In addition to these posttarget changes, the level of spontaneous spike activity during the pretarget period was negatively correlated with both neural and saccade latencies. These results demonstrate that V1 activity correlates with the gap effect and indicate that trial-to-trial variability in the state of V1 accompanies the variability of neural and behavioral latencies. NEW & NOTEWORTHY The link between neural activity in monkey primary visual cortex (V1) and visually guided behavioral response is confirmed with the gap saccade paradigm. Results indicated that the variability in neural latency of V1 spike activity correlates with the gap effect on saccade latency and that the trial-to-trial variability in the state of V1 before the onset of saccade target correlates with the variability in neural and behavioral latencies. [ABSTRACT FROM AUTHOR]

We examined the effects of delaying terminal visual feedback on the relative contribution of explicit and implicit components of adaptation to a visuomotor rotation. Participants practiced a 30° rotation while receiving terminal visual feedback with either a short (0 ms), medium (200 ms), or long (1500 ms) delay. Explicit and implicit adjustments were dissociated by a series of posttests. While overall adaptation did not differ significantly between groups, aftereffects progressively decreased with increasing feedback delay. Moreover, explicit knowledge of the rotation increased in both the medium and high delay groups relative to the short delay group, but did not differ between the former two. This finding of feedback delay differentially affecting implicit adjustments as indexed by aftereffects and conscious strategic corrections based on explicit knowledge of the transformation substantiates the importance of distinguishing implicit and explicit components of adaptation even with rotations of smaller size and emphasizes the need to consider time delays in the interpretation of adaptation experiments and potentially in the design of training environments. [ABSTRACT FROM AUTHOR]

In rodents, the medial aspect of the secondary motor cortex (M2) is known by other names, including medial agranular cortex (AGm), medial precentral cortex (PrCm), and frontal orienting field (FOF). As a subdivision of the medial prefrontal cortex (mPFC), M2 can be defined by a distinct set of afferent and efferent connections, microstimulation responses, and lesion outcomes. However, the behavioral role of M2 remains mysterious. Here, we focus on evidence from rodent studies, highlighting recent findings of early and context-dependent choice-related activity in M2 during voluntary behavior. Based on the current understanding, we suggest that a major function for M2 is to flexibly map antecedent signals such as sensory cues to motor actions, thereby enabling adaptive choice behavior. [ABSTRACT FROM AUTHOR]

How rapidly can the brain transform vision into action? Work in humans has established that the transformation for visually-guided reaching can be remarkably rapid, with the first phase of upper limb muscle recruitment, the express visuomotor response, beginning within less than 100 ms of visual target presentation. Such short-latency responses limit the opportunities for extensive cortical processing, leading to the hypothesis that they are generated via the subcortical tecto-reticulo-spinal pathway. Here, we examine whether nonhuman primates (NHPs) exhibit express visuomotor responses. Two male macaques made visually-guided reaches in a behavioral paradigm known to elicit express visuomotor responses in humans, while we acquired intramuscular recordings from the deltoid muscle. Across several variants of this paradigm, express visuomotor responses began within 65 ms (range: 48-91 ms) of target presentation. Although the timing of the express visuomotor response did not co-vary with reaction time, larger express visuomotor responses tended to precede shorter latency reaches. Further, we observed that the magnitude of the express visuomotor response could be muted by contextual context, although this effect was quite variable. Overall, the response properties in NHPs resemble those in humans. Our results establish a new benchmark for visuomotor transformations underlying visually-guided reaches, setting the stage for experiments that can directly compare the role of cortical and subcortical areas in reaching when time is of the essence., (Copyright © 2023 Cecala et al.)

New findings advance our understanding of how vision is used to guide the hand during object grasping.

Grasping requires translating object geometries into appropriate hand shapes. How the brain computes these transformations is currently unclear. We investigated three key areas of the macaque cortical grasping circuit with microelectrode arrays and found cooperative but anatomically separated visual and motor processes. The parietal area AIP operated primarily in a visual mode. Its neuronal population revealed a specialization for shape processing, even for abstract geometries, and processed object features ultimately important for grasping. Premotor area F5 acted as a hub that shared the visual coding of AIP only temporarily and switched to highly dominant motor signals towards movement planning and execution. We visualize these non-discrete premotor signals that drive the primary motor cortex M1 to reflect the movement of the grasping hand. Our results reveal visual and motor features encoded in the grasping circuit and their communication to achieve transformation for grasping.

To produce goal-directed eye movements known as saccades, we must channel sensory input from our environment through a process known as sensorimotor transformation. The behavioral output of this phenomenon (an accurate eye movement) is straightforward, but the coordinated activity of neurons underlying its dynamics is not well understood. We searched for a neural correlate of sensorimotor transformation in the activity patterns of simultaneously recorded neurons in the superior colliculus (SC) of three male rhesus monkeys performing a visually guided, delayed saccade task. Neurons in the intermediate layers produce a burst of spikes both following the appearance of a visual (sensory) stimulus and preceding an eye movement command, but many also exhibit a sustained activity level during the intervening time ("delay period"). This sustained activity could be representative of visual processing or motor preparation, along with countless cognitive processes. Using a novel measure we call the Visuomotor Proximity Index (VMPI), we pitted visual and motor signals against each other by measuring the degree to which each session's population activity (as summarized in a low-dimensional framework) could be considered more visual-like or more motor-like. The analysis highlighted two salient features of sensorimotor transformation. One, population activity on average drifted systematically toward a motor-like representation and intermittently reverted to a visual-like representation following a microsaccade. Two, activity patterns that drift to a stronger motor-like representation by the end of the delay period may enable a more rapid initiation of a saccade, substantiating the idea that this movement initiation mechanism is conserved across motor systems.

All animals use olfactory information to perform tasks essential to their survival. Odors typically activate multiple olfactory receptor neuron (ORN) classes and are therefore represented by the patterns of active ORNs. How the patterns of active ORN classes are decoded to drive behavior is under intense investigation. In this study, using Drosophila as a model system, we investigate the logic by which odors modulate locomotion. We designed a novel behavioral arena in which we could examine a fly’s locomotion under precisely controlled stimulus condition. In this arena, in response to similarly attractive odors, flies modulate their locomotion differently implying that odors have a more diverse effect on locomotion than was anticipated. Three features underlie odor-guided locomotion: First, in response to odors, flies modulate a surprisingly large number of motor parameters. Second, similarly attractive odors elicit changes in different motor programs. Third, different ORN classes modulate different subset of motor parameters.

To reach for an object, we must convert its spatial location into an appropriate motor command, merging movement direction and amplitude. In humans, it has been suggested that this visuo-motor transformation occurs in a dorsomedial parieto-frontal pathway, although the causal contribution of the areas constituting the reaching circuit remains unknown. Here we used transcranial magnetic stimulation (TMS) in healthy volunteers to disrupt the function of either the medial intraparietal area (mIPS) or dorsal premotor cortex (PMd), in each hemisphere. The task consisted in performing step-tracking movements with the right wrist towards targets located in different directions and eccentricities; the targets were either visible for the whole trial (Target-ON) or flashed for 200 ms (Target-OFF). Left and right mIPS disruption led to errors in the initial direction of movements performed towards contralateral targets. These errors were corrected online in the Target-ON condition but when the target was flashed for 200 ms, mIPS TMS manifested as a larger endpoint spreading. In contrast, left PMd virtual lesions led to higher acceleration and velocity peaks - two parameters typically used to probe the planned movement amplitude - irrespective of the target position, hemifield and presentation condition; in the Target-OFF condition, left PMd TMS induced overshooting and increased the endpoint dispersion along the axis of the target direction. These results indicate that left PMd intervenes in coding amplitude during movement preparation. The critical TMS timings leading to errors in direction and amplitude were different, namely 160-100 ms before movement onset for mIPS and 100-40 ms for left PMd. TMS applied over right PMd had no significant effect. These results indicate that, during motor preparation, direction and amplitude of goal-directed movements are processed by different cortical areas, at distinct timings, and according to a specific hemispheric organization.

The neural circuits in the optic tectum of Xenopus tadpoles are selectively responsive to looming visual stimuli that resemble objects approaching the animal at a collision trajectory. This selectivity is required for adaptive collision avoidance behavior in this species, but its underlying mechanisms are not known. In particular, it is still unclear how the balance between the recurrent spontaneous network activity and the newly arriving sensory flow is set in this structure, and to what degree this balance is important for collision detection. Also, despite the clear indication for the presence of strong recurrent excitation and spontaneous activity, the exact topology of recurrent feedback circuits in the tectum remains elusive. In this study we take advantage of recently published detailed cell-level data from tadpole tectum to build an informed computational model of it, and investigate whether dynamic activation in excitatory recurrent retinotopic networks may on its own underlie collision detection. We consider several possible recurrent connectivity configurations and compare their performance for collision detection under different levels of spontaneous neural activity. We show that even in the absence of inhibition, a retinotopic network of quickly inactivating spiking neurons is naturally selective for looming stimuli, but this selectivity is not robust to neuronal noise, and is sensitive to the balance between direct and recurrent inputs. We also describe how homeostatic modulation of intrinsic properties of individual tectal cells can change selectivity thresholds in this network, and qualitatively verify our predictions in a behavioral experiment in freely swimming tadpoles. [ABSTRACT FROM AUTHOR]

The perception of objects does not rely only on visual brain areas, but also involves cortical motor regions. In particular, different parietal and premotor areas host neurons discharging during both object observation and grasping. Most of these cells often show similar visual and motor selectivity for a specific object (or set of objects), suggesting that they might play a crucial role in representing the potential motor act afforded by the object. The existence of such a mechanism for the visuomotor transformation of object physical properties in the most appropriate motor plan for interacting with them has been convincingly demonstrated in humans as well. Interestingly, human studies have shown that visually presented objects can automatically trigger the representation of an action provided that they are located within the observer’s reaching space (peripersonal space). The affordance effect also occurs when the presented object is outside the observer’s peripersonal space, but inside the peripersonal space of an observed agent. These findings recently received direct support by single neuron studies in monkey, indicating that space-constrained processing of objects in the ventral premotor cortex might be relevant to represent objects as potential targets for one’s own or others' action.

When using lever tools, subjects have to deal with two, not necessarily concordant effects of their motor behavior: The body-related proximal effects, like tactile sensations from the moving hand, and/or more external distal effects, like the moving effect points of the lever. As a consequence, spatial compatibility relationships between stimulus (S; at which the effect points of the lever aim at), responding hand (R) and effect point of the lever (E) play a critical role in response generation. In the present study we examine whether the occurrence of compatibility effects needs real tool movements or whether a similar response pattern can be already evoked by pure mental imaginations of the tool effects. In general, response times and errors observed with real and imagined tool movements showed a similar pattern of results, but there were also differences. With incompatible relationships and thus more difficult tasks, response times were reduced with imagined tool movements than compared with real tool movements. On the contrary, with compatible relationships and thus high overlap between proximal and distal action effects, response times were increased with imagined tool movements. Results are only in parts consistent with the ideomotor theory of motor control.

Both fronto-parietal networks and the basal ganglia play an important role in action cascading. It is well-known that cortical structures mediate sensorimotor transformation for this purpose. The striatum receives extensive input from those cortical structures and has been shown to be modulated by the predictability of cortical input. Until today, it has however remained unclear whether the processing of spatial codes or even sensorimotor transformation processes for the purpose of action cascading involve the striatum. We therefore examined this question by means of fMRI using a stop-change task that varied the predictability as well as the complexity of sensorimotor transformations required for correct responding in the context of action cascading. On the behavioral level, we found that the complexity of sensorimotor transformation processes only prolonged reaction times when the requirement for this transformation was predictable. fMRI results matched this effect showing enhanced activity of the caudate in case a complex sensorimotor transformation could be anticipated. Irrespective of the complexity of the required transformations, the putamen was furthermore involved in the prediction of imminent action cascading demands. Taken together, our findings give rise to a conceptual advance regarding basal ganglia function by showing that the anticipation and, more importantly, processing of complex sensorimotor transformation processes involves the striatum. [ABSTRACT FROM AUTHOR]

Sensory events in the space around us trigger specific motor patterns directed toward or away from the spatial location of the sensory source. Spatially-defined sensorimotor associations are well-known in the visual domain but less so for the auditory modality. In particular no spatially-directed audio-motor association has been described for the upper limb. We tested the instantaneous directional tuning of the corticospinal system by means of single-pulse transcranial magnetic stimulation (TMS) over the left motor cortex in 16 healthy volunteers while at rest. We recorded the lateral accelerations of the TMS-evoked movement by means of an accelerometer placed on the forearm. Acoustic stimuli (pure tone frequency = 1000 Hz, duration = 50 ms) coming from 25 different directions lying in the axial anterior half-plane at the height of the participant’s ears were played on earphones. The entire set of sound directions covered a span of 160° (±80° where 0° is the frontal direction) at a fixed azimuth angle. Six different intervals between sound onset and TMS (0, 25, 50, 100, 150 and 200 ms) were tested for each sound direction. Significant correlations were found between sound origin and TMS-evoked arm accelerations only when TMS was delivered 50 ms prior to sound onset. We show the presence in the upper limb motor system of auditory spatial tuning. Sound information accesses the motor system at very short latency, potentially compatible with both a subcortical and a cortical origin of the response. The use of TMS-evoked accelerations allowed us to disclose a strict directional tuning in audio-motor associations. [ABSTRACT FROM AUTHOR]

Active eye movements can be exploited to build a visuomotor representation of the surrounding environment. Maintaining and improving such representation requires to update the internal model involved in the generation of eye movements. From this perspective, action and perception are thus tightly coupled and interdependent. In this work, we encoded the internal model for oculomotor control with an adaptive filter inspired by the functionality of the cerebellum. Recurrent loops between a feed-back controller and the internal model allow our system to perform accurate binocular saccades and create an implicit representation of the nearby space. Simulation results show that this recurrent architecture outperforms classical feedback-error-learning in terms of both accuracy and sensitivity to system parameters. The proposed approach was validated implementing the framework on an anthropomorphic robotic head. [ABSTRACT FROM AUTHOR]

Humans and other primates possess a unique capacity to grasp and manipulate objects skillfully, a facility pervasive in everyday life that has undoubtedly contributed to the success of our species. When we reach and grasp an object, various cortical areas in the parietal and frontal lobes work together effortlessly to analyze object shape and position, transform this visual information into useful motor commands, and implement these motor representations to preshape the hand before contact with the object is made. In recent years, a growing number of studies have investigated the neural circuits underlying object grasping in both the visual and motor systems of the macaque monkey. The accumulated knowledge not only helps researchers understand how object grasping is implemented in the primate brain but may also contribute to the development of novel neural interfaces and neuroprosthetics. [ABSTRACT FROM AUTHOR]

Driver behavior and vehicle-road kinematics have been shown to change over prolonged periods of driving; however, the interaction between these two indices has not been examined. Here we develop a measure that examines how drivers turn the steering wheel relative to heading error velocity, which the authors call the relative steering wheel compensation (RSWC). The RSWC transiently changes on a short time scale coincident with a verbal query embedded within the study paradigm. In contrast, more traditional variables are dynamic over longer time scales consistent with previous research. The results suggest drivers alter their behavioral output (steering wheel correction) relative to sensory input (vehicle heading error velocity) on a distinct temporal scale and may reflect an interaction of alerting and control. [ABSTRACT FROM AUTHOR]

The article explores the possibilities of formalizing and explaining the mechanisms that support spatial and social perspective alignment sustained over the duration of a social interaction. The basic proposed principle is that in social contexts the mechanisms for sensorimotor transformations and multisensory integration (learn to) incorporate information relative to the other actor(s), similar to the "re-calibration" of visual receptive fields in response to repeated tool use. This process aligns or merges the co-actors' spatial representations and creates a "Shared Action Space" supporting key computations of social interactions and joint actions; for example, the remapping between the coordinate systems and frames of reference of the co-actors, including perspective taking, the sensorimotor transformations required for lifting jointly an object, and the predictions of the sensory effects of such joint action. The social re-calibration is proposed to be based on common basis function maps and could constitute an optimal solution to sensorimotor transformation and multisensory integration in joint action or more in general social interaction contexts. However, certain situations such as discrepant postural and viewpoint alignment and associated differences in perspectives between the co-actors could constrain the process quite differently. We discuss how alignment is achieved in the first place, and how it is maintained over time, providing a taxonomy of various forms and mechanisms of space alignment and overlap based, for instance, on automaticity vs. control of the transformations between the two agents. Finally, we discuss the link between low-level mechanisms for the sharing of space and high-level mechanisms for the sharing of cognitive representations.