Largely shared neural codes for biological and nonbiological observed movements but not for executed actions in monkey premotor areas

The neural processing of others' observed actions recruits a large network of brain regions (the action observation network, AON), in which frontal motor areas are thought to play a crucial role. Since the discovery of mirror neurons (MNs) in the ventral premotor cortex, it has been assumed that their activation was conditional upon the presentation of biological rather than nonbiological motion stimuli, supporting a form of direct visuomotor matching. Nonetheless, nonbiological observed movements have rarely been used as control stimuli to evaluate visual specificity, thereby leaving the issue of similarity among neural codes for executed actions and biological or nonbiological observed movements unresolved. Here, we addressed this issue by recording from two nodes of the AON that are attracting increasing interest, namely the ventro-rostral part of the dorsal premotor area F2 and the mesial pre-supplementary motor area F6 of macaques while they 1) executed a reaching-grasping task, 2) observed an experimenter performing the task, and 3) observed a nonbiological effector moving in the same context. Our findings revealed stronger neuronal responses to the observation of biological than nonbiological movement, but biological and nonbiological visual stimuli produced highly similar neural dynamics and relied on largely shared neural codes, which in turn remarkably differed from those associated with executed actions. These results indicate that, in highly familiar contexts, visuo-motor remapping processes in premotor areas hosting MNs are more complex and flexible than predicted by a direct visuomotor matching hypothesis.

Dorsal Prefrontal Cortex

The dorsal prefrontal (PF) cortex generates and plans the goals or targets for foveal search and manual foraging. The goals are conditional on the relative recency of prior events and actions, and the connections of areas 9/46 and 46 explain how these areas can support the ability to generate the next goal. Area 9/46 can generate sequences of eye movements because it has visuospatial inputs from the cortex in the intraparietal sulcus and outputs to the frontal eye field and superior colliculus. Area 46 can generate sequences of hand and arm movements because it has inputs from the inferior parietal areas PFG and SII and outputs to the forelimb regions of the premotor areas and thence to the motor cortex. Both areas get timing and order information indirectly from the parietal cortex and hippocampus, and colour and shape information from the ventral prefrontal cortex. Inputs from the orbital prefrontal cortex enable both areas to integrate generate goals in accordance with current needs.

Medial Prefrontal Cortex

In primates, the medial prefrontal cortex (PF) supports sequences of self-generated actions that are performed spontaneously and without external cues to instruct the action that is appropriate. Instead, the actions are performed on the basis of memories of previous events and their outcomes. Inputs from the parahippocampal and hippocampal cortex provide information about the scene or context; and inputs from the amygdala and orbital prefrontal cortex specify the outcomes. In ancestral anthropoids the hippocampal system for navigation was co-opted to support the retrieval of sequences of actions performed with the hand and arm, as in foraging. Outputs to the medial premotor areas influence the choice of actions, either for exploiting current resources or for exploring so as to find new ones. In anthropoids, visual and auditory inputs also convey the actions of conspecifics and predators so that the animal can predict what others are going to do.

The neuroscience of groove: neural mechanisms marrying music and movement

Music has a long history of being associated with movement synchronization such as foot-tapping or dance. These behaviours are easier with some music compared to others, and the reasons for this are not well understood. Groove is a quality of music that compels synchronous movement in the listener, and certain acoustic and musical features have been identified that contribute to a sense of groove.Neurons have been found to entrain to the beat of music. Combining these two ideas, it is reasonable to predict that neural populations involved in movement (i.e. premotor areas) would entrain more to high-groove than to low-groove music. This dissertation explores some of the psychological, musical and acoustic aspects of music that contribute to neural entrainment in premotor areas of the brain. Study 1 investigates the effects of feelings of groove on pre-motor entrainment, using stimuli that have been rated on extent of groove in a previous study. Study 2 investigates the musical feature of syncopation – which has previously been found to be associated with sense of groove – on extent of premotor entrainment and behavioural synchronization ability. Study 3 investigates the effects of acoustic features that have been found to be related to groove and movement synchronization such as event density and percussiveness. The pattern of results across all studies suggests that the complexity of the rhythms in the stimulus determines the extent of beat entrainment. Feelings of groove, however, are better characterized by “beat complexity”, which depends on a) the extent to which the listener perceives the beat, and b) the extent to which other rhythmic elements of the music compete with the beat. A network of brain areas integral to the perception of groove is proposed, where activation of premotor areas enables music to drive motor output.

The neuroscience of groove: neural mechanisms marrying music and movement

Music has a long history of being associated with movement synchronization such as foot-tapping or dance. These behaviours are easier with some music compared to others, and the reasons for this are not well understood. Groove is a quality of music that compels synchronous movement in the listener, and certain acoustic and musical features have been identified that contribute to a sense of groove.Neurons have been found to entrain to the beat of music. Combining these two ideas, it is reasonable to predict that neural populations involved in movement (i.e. premotor areas) would entrain more to high-groove than to low-groove music. This dissertation explores some of the psychological, musical and acoustic aspects of music that contribute to neural entrainment in premotor areas of the brain. Study 1 investigates the effects of feelings of groove on pre-motor entrainment, using stimuli that have been rated on extent of groove in a previous study. Study 2 investigates the musical feature of syncopation – which has previously been found to be associated with sense of groove – on extent of premotor entrainment and behavioural synchronization ability. Study 3 investigates the effects of acoustic features that have been found to be related to groove and movement synchronization such as event density and percussiveness. The pattern of results across all studies suggests that the complexity of the rhythms in the stimulus determines the extent of beat entrainment. Feelings of groove, however, are better characterized by “beat complexity”, which depends on a) the extent to which the listener perceives the beat, and b) the extent to which other rhythmic elements of the music compete with the beat. A network of brain areas integral to the perception of groove is proposed, where activation of premotor areas enables music to drive motor output.

Afferent connections of cytoarchitectural area 6M and surrounding cortex in the marmoset: putative homologues of the supplementary and pre-supplementary motor areas

Cortical projections to the caudomedial frontal cortex were studied using retrograde tracers in marmosets. We tested the hypothesis that cytoarchitectural area 6M includes homologues of the supplementary and pre-supplementary motor areas (SMA and preSMA) of other primates. We found that, irrespective of the injection sites' location within 6M, over half of the labeled neurons were located in motor and premotor areas. Other connections originated in prefrontal area 8b, ventral anterior and posterior cingulate areas, somatosensory areas (3a and 1-2), and areas on the rostral aspect of the dorsal posterior parietal cortex. Although the origin of afferents was similar, injections in rostral 6M received higher percentages of prefrontal afferents, and fewer somatosensory afferents, compared to caudal injections, compatible with differentiation into SMA and preSMA. Injections rostral to 6M (area 8b) revealed a very different set of connections, with increased emphasis in prefrontal and posterior cingulate afferents, and fewer parietal afferents. The connections of 6M were also quantitatively different from those of M1, dorsal premotor areas, and cingulate motor area 24d. These results show that the cortical motor control circuit is conserved in simian primates, indicating that marmosets can be valuable models for studying movement planning and control.

Fast-spiking interneurons of the premotor cortex contribute to action planning

Planning and execution of voluntary movement depend on the contribution of distinct classes of neurons in primary motor and premotor areas. However, the specific functional role of GABAergic cells remains only partly understood. Here, electrophysiological and computational analyses are employed to compare directly the response properties of putative pyramidal (PNs) and fast-spiking, GABAergic neurons (FSNs) during licking and forelimb retraction in mice. Recordings from anterolateral motor cortex and rostral forelimb area, reveal that FSNs fire earlier and for a longer duration than PNs, with the exception of a subset of early-modulated PNs in deep layers. Computational analysis reveals that FSNs carry vastly more information than PNs about the onset of movement. While PNs differently modulate their discharge during distinct motor acts, most FSNs respond with a stereotyped increase in firing rate. Accordingly, the informational redundancy was greater among FSNs than PNs. These data suggest that a global rise of inhibition contributes to early action planning.

Neural Correlates of Hand–Object Congruency Effects during Action Planning

Selecting hand actions to manipulate an object is affected both by perceptual factors and by action goals. Affordances may contribute to “stimulus–response” congruency effects driven by habitual actions to an object. In previous studies, we have demonstrated an influence of the congruency between hand and object orientations on response times when reaching to turn an object, such as a cup. In this study, we investigated how the representation of hand postures triggered by planning to turn a cup was influenced by this congruency effect, in an fMRI scanning environment. Healthy participants were asked to reach and turn a real cup that was placed in front of them either in an upright orientation or upside–down. They were instructed to use a hand orientation that was either congruent or incongruent with the cup orientation. As expected, the motor responses were faster when the hand and cup orientations were congruent. There was increased activity in a network of brain regions involving object-directed actions during action planning, which included bilateral primary and extrastriate visual, medial, and superior temporal areas, as well as superior parietal, primary motor, and premotor areas in the left hemisphere. Specific activation of the dorsal premotor cortex was associated with hand–object orientation congruency during planning and prior to any action taking place. Activity in that area and its connectivity with the lateral occipito-temporal cortex increased when planning incongruent (goal-directed) actions. The increased activity in premotor areas in trials where the orientation of the hand was incongruent to that of the object suggests a role in eliciting competing representations specified by hand postures in lateral occipito-temporal cortex.

Functional Lateralization of the Mirror Neuron System in Monkey and Humans

To date, both in monkeys and humans, very few studies have addressed the issue of the lateralization of the cortical parietal and premotor areas involved in the organization of voluntary movements and in-action understanding. In this review, we will first analyze studies in the monkey, describing the functional properties of neurons of the parieto-frontal circuits, involved in the organization of reaching-grasping actions, in terms of unilateral or bilateral control. We will concentrate, in particular, on the properties of the mirror neuron system (MNS). Then, we will consider the evidence about the mirror neuron mechanism in humans, describing studies in which action perception, as well as action execution, produces unilateral or bilateral brain activation. Finally, we will report some investigations demonstrating plastic changes of the MNS following specific unilateral brain damage, discussing how this plasticity can be related to the rehabilitation outcome