Laminar differences in decision-related neural activity in dorsal premotor cortex.
ABSTRACT: Dorsal premotor cortex is implicated in somatomotor decisions. However, we do not understand the temporal patterns and laminar organization of decision-related firing rates in dorsal premotor cortex. We recorded neurons from dorsal premotor cortex of monkeys performing a visual discrimination task with reaches as the behavioral report. We show that these neurons can be organized along a bidirectional visuomotor continuum based on task-related firing rates. "Increased" neurons at one end of the continuum increased their firing rates ~150?ms after stimulus onset and these firing rates covaried systematically with choice, stimulus difficulty, and reaction time-characteristics of a candidate decision variable. "Decreased" neurons at the other end of the continuum reduced their firing rate after stimulus onset, while "perimovement" neurons at the center of the continuum responded only ~150?ms before movement initiation. These neurons did not show decision variable-like characteristics. "Increased" neurons were more prevalent in superficial layers of dorsal premotor cortex; deeper layers contained more "decreased" and "perimovement" neurons. These results suggest a laminar organization for decision-related responses in dorsal premotor cortex.Dorsal premotor cortex (PMd) is thought to be involved in making somatomotor decisions. Chandrasekaran et al. investigated the temporal response dynamics of PMd neurons across cortical layers and show stronger and earlier decision-related responses in the superficial layers and more action execution-related signals in the deeper layers.
Project description:Dorsal premotor cortex (PMd) is known to be involved in the planning and execution of reaching movements. However, it is not understood how PMd plan activity-often present in the very same neurons that respond during movement-is prevented from itself producing movement. We investigated whether inhibitory interneurons might "gate" output from PMd, by maintaining high levels of inhibition during planning and reducing inhibition during execution. Recently developed methods permit distinguishing interneurons from pyramidal neurons using extracellular recordings. We extend these methods here for use with chronically implanted multi-electrode arrays. We then applied these methods to single- and multi-electrode recordings in PMd of two monkeys performing delayed-reach tasks. Responses of putative interneurons were not generally in agreement with the hypothesis that they act to gate output from the area: in particular it was not the case that interneurons tended to reduce their firing rates around the time of movement. In fact, interneurons increased their rates more than putative pyramidal neurons during both the planning and movement epochs. The two classes of neurons also differed in a number of other ways, including greater modulation across conditions for interneurons, and interneurons more frequently exhibiting increases in firing rate during movement planning and execution. These findings provide novel information about the greater responsiveness of putative PMd interneurons in motor planning and execution and suggest that we may need to consider new possibilities for how planning activity is structured such that it does not itself produce movement.
Project description:Classically, it has been hypothesized that reach-to-grasp movements arise from two discrete parietofrontal cortical networks. As part of these networks, the dorsal premotor cortex (PMd) has been implicated in the control of reaching movements of the arm, whereas the ventral premotor cortex (PMv) has been associated with the control of grasping movements of the hand. Recent studies have shown that such a strict delineation of function along anatomical boundaries is unlikely, partly because reaching to different locations can alter distal hand kinematics and grasping different objects can affect kinematics of the proximal arm. Here, we used chronically implanted multielectrode arrays to record unit-spiking activity in both PMd and PMv simultaneously while rhesus macaques engaged in a reach-to-grasp task. Generalized linear models were used to predict the spiking activity of cells in both areas as a function of different kinematic parameters, as well as spike history. To account for the influence of reaching on hand kinematics and vice versa, we applied demixed principal components analysis to define kinematics synergies that maximized variance across either different object locations or grip types. We found that single cells in both PMd and PMv encode the kinematics of both reaching and grasping synergies, suggesting that this classical division of reach and grasp in PMd and PMv, respectively, does not accurately reflect the encoding preferences of cells in those areas.SIGNIFICANCE STATEMENT For reach-to-grasp movements, the dorsal premotor cortex (PMd) has been implicated in the control of reaching movements of the arm, whereas the ventral premotor cortex (PMv) has been associated with the control of grasping movements of the hand. We recorded unit-spiking activity in PMd and PMv simultaneously while macaques performed a reach-to-grasp task. We modeled the spiking activity of neurons as a function of kinematic parameters and spike history. We applied demixed principal components analysis to define kinematics synergies. We found that single units in both PMd and PMv encode the kinematics of both reaching and grasping synergies, suggesting that the division of reach and grasp in PMd and PMv, respectively, cannot be made based on their encoding properties.
Project description:Our brain continuously receives information over multiple timescales that are differently processed across areas. In this study, we investigated the intrinsic timescale of neurons in the dorsal premotor cortex (PMd) of two rhesus macaques while performing a non-match-to-goal task. The task rule was to reject the previously chosen target and select the alternative one. We defined the intrinsic timescale as the decay constant of the autocorrelation structure computed during a baseline period of the task. We found that neurons with longer intrinsic timescale tended to maintain a stronger spatial response coding during a delay period. This result suggests that longer intrinsic timescales predict the functional role of PMd neurons in a cognitive task. Our estimate of the intrinsic timescale integrates an existing hierarchical model (Murray et al., 2014), by assigning to PMd a lower position than prefrontal cortex in the hierarchical ordering of the brain areas based on neurons' timescales.
Project description:Rewards associated with actions are critical for motivation and learning about the consequences of one's actions on the world. The motor cortices are involved in planning and executing movements, but it is unclear whether they encode reward over and above limb kinematics and dynamics. Here, we report a categorical reward signal in dorsal premotor (PMd) and primary motor (M1) neurons that corresponds to an increase in firing rates when a trial was not rewarded regardless of whether or not a reward was expected. We show that this signal is unrelated to error magnitude, reward prediction error, or other task confounds such as reward consumption, return reach plan, or kinematic differences across rewarded and unrewarded trials. The availability of reward information in motor cortex is crucial for theories of reward-based learning and motivational influences on actions.
Project description:BACKGROUND: The lateral premotor cortex plays a crucial role in visually guided limb movements. It is divided into two main regions, the dorsal (PMd) and ventral (PMv) areas, which are in turn subdivided into functionally and anatomically distinct rostral (PMd-r and PMv-r) and caudal (PMd-c and PMv-c) sub-regions. We analyzed the callosal inputs to these premotor subdivisions following 23 injections of retrograde tracers in eight macaque monkeys. In each monkey, 2-4 distinct tracers were injected in different areas allowing direct comparisons of callosal connectivity in the same brain. RESULTS: Based on large injections covering the entire extent of the corresponding PM area, we found that each area is strongly connected with its counterpart in the opposite hemisphere. Callosal connectivity with the other premotor areas, the primary motor cortex, prefrontal cortex and somatosensory cortex varied from one area to another. The most extensive callosal inputs terminate in PMd-r and PMd-c, with PMd-r strongly connected with prefrontal cortex. Callosal inputs to PMv-c are more extensive than those to PMv-r, whose connections are restricted to its counterpart area. Quantitative analysis of labelled cells confirms these general findings, and allows an assessment of the relative strength of callosal inputs. CONCLUSION: PMd-r and PMv-r receive their strongest callosal inputs from their respective counterpart areas, whereas PMd-c and PMv-c receive strong inputs from heterotopic areas as well (namely from PMd-r and PMv-r, respectively). Finally, PMd-r stands out as the lateral premotor area with the strongest inputs from the prefrontal cortex, and only the PMd-c and PMv-c receive weak callosal inputs from M1.
Project description:Our bodies and the environment constrain our movements. For example, when our arm is fully outstretched, we cannot extend it further. More generally, the distribution of possible movements is conditioned on the state of our bodies in the environment, which is constantly changing. However, little is known about how the brain represents such distributions, and uses them in movement planning. Here, we record from dorsal premotor cortex (PMd) and primary motor cortex (M1) while monkeys reach to randomly placed targets. The hand's position within the workspace creates probability distributions of possible upcoming targets, which affect movement trajectories and latencies. PMd, but not M1, neurons have increased activity when the monkey's hand position makes it likely the upcoming movement will be in the neurons' preferred directions. Across the population, PMd activity represents probability distributions of individual upcoming reaches, which depend on rapidly changing information about the body's state in the environment.
Project description:Every movement we make represents one of many possible actions. In reaching tasks with multiple targets, dorsal premotor cortex (PMd) appears to represent all possible actions simultaneously. However, in many situations we are not presented with explicit choices. Instead, we must estimate the best action based on noisy information and execute it while still uncertain of our choice. Here we asked how both primary motor cortex (M1) and PMd represented reach direction during a task in which a monkey made reaches based on noisy, uncertain target information. We found that with increased uncertainty, neurons in PMd actually enhanced their representation of unlikely movements throughout both planning and execution. The magnitude of this effect was highly variable across sessions, and was correlated with a measure of the monkeys' behavioral uncertainty. These effects were not present in M1. Our findings suggest that PMd represents and maintains a full distribution of potentially correct actions.
Project description:Spatial computations underlying the coordination of the hand and eye present formidable geometric challenges. One way for the nervous system to simplify these computations is to directly encode the relative position of the hand and the center of gaze. Neurons in the dorsal premotor cortex (PMd), which is critical for the guidance of arm-reaching movements, encode the relative position of the hand, gaze, and goal of reaching movements. This suggests that PMd can coordinate reaching movements with eye movements. Here, we examine saccade-related signals in PMd to determine whether they also point to a role for PMd in coordinating visual-motor behavior. We first compared the activity of a population of PMd neurons with a population of parietal reach region (PRR) neurons. During center-out reaching and saccade tasks, PMd neurons responded more strongly before saccades than PRR neurons, and PMd contained a larger proportion of exclusively saccade-tuned cells than PRR. During a saccade relative position-coding task, PMd neurons encoded saccade targets in a relative position code that depended on the relative position of gaze, the hand, and the goal of a saccadic eye movement. This relative position code for saccades is similar to the way that PMd neurons encode reach targets. We propose that eye movement and eye position signals in PMd do not drive eye movements, but rather provide spatial information that links the control of eye and arm movements to support coordinated visual-motor behavior.
Project description:Despite the common conception of the dorsal premotor cortex (PMd) as a single brain region, its diverse connectivity profiles and behavioral heterogeneity argue for a differentiated organization of the PMd. A previous study revealed that the right PMd is characterized by a rostro-caudal and a ventro-dorsal distinction dividing it into five subregions: rostral, central, caudal, ventral and dorsal. The present study assessed whether a similar organization is present in the left hemisphere, by capitalizing on a multimodal data-driven approach combining connectivity-based parcellation (CBP) based on meta-analytic modeling, resting-state functional connectivity, and probabilistic diffusion tractography. The resulting PMd modules were then characterized based on multimodal functional connectivity and a quantitative analysis of associated behavioral functions. Analyzing the clusters consistent across all modalities revealed an organization of the left PMd that mirrored its right counterpart to a large degree. Again, caudal, central and rostral modules reflected a cognitive-motor gradient and a premotor eye-field was found in the ventral part of the left PMd. In addition, a distinct module linked to abstract cognitive functions was observed in the rostro-ventral left PMd across all CBP modalities, implying greater differentiation of higher cognitive functions for the left than the right PMd.
Project description:How deliberation on sensory cues and action selection interact in decision-related brain areas is still not well understood. Here, monkeys reached to one of two targets, whose colors alternated randomly between trials, by discriminating the dominant color of a checkerboard cue composed of different numbers of squares of the two target colors in different trials. In a Targets First task the colored targets appeared first, followed by the checkerboard; in a Checkerboard First task, this order was reversed. After both cues appeared in both tasks, responses of dorsal premotor cortex (PMd) units covaried with action choices, strength of evidence for action choices, and RTs- hallmarks of decision-related activity. However, very few units were modulated by checkerboard color composition or the color of the chosen target, even during the checkerboard deliberation epoch of the Checkerboard First task. These findings implicate PMd in the action-selection but not the perceptual components of the decision-making process in these tasks.