Intrinsic functional clustering of ventral premotor F5 in the macaque brain

© 2020 Neurophysiological and anatomical data suggest the existence of several functionally distinct regions in the lower arcuate sulcus and adjacent postarcuate convexity of the macaque monkey. Ventral premotor F5c lies on the postarcuate convexity and consists of a dorsal hand-related and ventral mouth-related field. The posterior bank of the lower arcuate contains two additional premotor F5 subfields at different anterior-posterior levels, F5a and F5p. Anterior to F5a, area 44 has been described as a dysgranular zone occupying the deepest part of the fundus of the inferior arcuate. Finally, area GrFO occupies the most rostral portion of the fundus and posterior bank of inferior arcuate and extends ventrally onto the frontal operculum. Recently, data-driven exploratory approaches using resting-state fMRI data have been suggested as a promising non-invasive method for examining the functional organization of the primate brain. Here, we examined to what extent partitioning schemes derived from data-driven clustering analysis of resting-state fMRI data correspond with the proposed organization of the fundus and posterior bank of the macaque arcuate sulcus, as suggested by invasive architectonical, connectional and functional investigations. Using a hierarchical clustering analysis, we could retrieve clusters corresponding to the dorsal and ventral portions of F5c on the postarcuate convexity, F5a and F5p at different antero-posterior locations on the posterior bank of the lower arcuate, area 44 in the fundus, as well as part of area GrFO in the most anterior portion of the fundus. Additionally, each of these clusters displayed distinct whole-brain functional connectivity, in line with previous anatomical tracer and seed-based functional connectivity investigations of F5/44 subdivisions. Overall, our data suggests that hierarchical clustering analysis of resting-state fMRI data can retrieve a fine-grained level of cortical organization that resembles detailed parcellation schemes derived from invasive functional and anatomical investigations

From language comprehension to action understanding and back again

A controversial question in cognitive neuroscience is whether comprehension of words and sentences engages brain mechanisms specific for decoding linguistic meaning or whether language comprehension occurs through more domain-general sensorimotor processes. Accumulating behavioral and neuroimaging evidence suggests a role for cortical motor and premotor areas in passive action-related language tasks, regions that are known to be involved in action execution and observation. To examine the involvement of these brain regions in language and nonlanguage tasks, we used functional magnetic resonance imaging (fMRI) on a group of 21 healthy adults. During the fMRI session, all participants 1) watched short object-related action movies, 2) looked at pictures of man-made objects, and 3) listened to and produced short sentences describing object-related actions and man-made objects. Our results are among the first to reveal, in the human brain, a functional specialization within the ventral premotor cortex (PMv) for observing actions and for observing objects, and a different organization for processing sentences describing actions and objects. These findings argue against the strongest version of the simulation theory for the processing of action-related language

Gestures, Vocalizations, and Memory in Language Origins

This article discusses the possible homologies between the human language networks and comparable auditory projection systems in the macaque brain, in an attempt to reconcile two existing views on language evolution: one that emphasizes hand control and gestures, and the other that emphasizes auditory–vocal mechanisms. The capacity for language is based on relatively well defined neural substrates whose rudiments have been traced in the non-human primate brain. At its core, this circuit constitutes an auditory–vocal sensorimotor circuit with two main components, a “ventral pathway” connecting anterior auditory regions with anterior ventrolateral prefrontal areas, and a “dorsal pathway” connecting auditory areas with parietal areas and with posterior ventrolateral prefrontal areas via the arcuate fasciculus and the superior longitudinal fasciculus. In humans, the dorsal circuit is especially important for phonological processing and phonological working memory, capacities that are critical for language acquisition and for complex syntax processing. In the macaque, the homolog of the dorsal circuit overlaps with an inferior parietal–premotor network for hand and gesture selection that is under voluntary control, while vocalizations are largely fixed and involuntary. The recruitment of the dorsal component for vocalization behavior in the human lineage, together with a direct cortical control of the subcortical vocalizing system, are proposed to represent a fundamental innovation in human evolution, generating an inflection point that permitted the explosion of vocal language and human communication. In this context, vocal communication and gesturing have a common history in primate communication

Grasp-specific motor resonance is influenced by the visibility of the observed actor

Motor resonance is the modulation of M1 corticospinal excitability induced by observation of others' actions. Recent brain imaging studies have revealed that viewing videos of grasping actions led to a differential activation of the ventral premotor cortex depending on whether the entire person is viewed versus only their disembodied hand. Here we used transcranial magnetic stimulation (TMS) to examine motor evoked potentials (MEPs) in the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) during observation of videos or static images in which a whole person or merely the hand was seen reaching and grasping a peanut (precision grip) or an apple (whole hand grasp). Participants were presented with six visual conditions in which visual stimuli (video vs static image), view (whole person vs hand) and grasp (precision grip vs whole hand grasp) were varied in a 2 × 2 × 2 factorial design. Observing videos, but not static images, of a hand grasping different objects resulted in a grasp-specific interaction, such that FDI and ADM MEPs were differentially modulated depending on the type of grasp being observed (precision grip vs whole hand grasp). This interaction was present when observing the hand acting, but not when observing the whole person acting. Additional experiments revealed that these results were unlikely to be due to the relative size of the hand being observed. Our results suggest that observation of videos rather than static images is critical for motor resonance. Importantly, observing the whole person performing the action abolished the grasp-specific effect, which could be due to a variety of PMv inputs converging on M1

Cortico-spinal modularity in the parieto-frontal system: a new perspective on action control

: Classical neurophysiology suggests that the motor cortex (MI) has a unique role in action control. In contrast, this review presents evidence for multiple parieto-frontal spinal command modules that can bypass MI. Five observations support this modular perspective: (i) the statistics of cortical connectivity demonstrate functionally-related clusters of cortical areas, defining functional modules in the premotor, cingulate, and parietal cortices; (ii) different corticospinal pathways originate from the above areas, each with a distinct range of conduction velocities; (iii) the activation time of each module varies depending on task, and different modules can be activated simultaneously; (iv) a modular architecture with direct motor output is faster and less metabolically expensive than an architecture that relies on MI, given the slow connections between MI and other cortical areas; (v) lesions of the areas composing parieto-frontal modules have different effects from lesions of MI. Here we provide examples of six cortico-spinal modules and functions they subserve: module 1) arm reaching, tool use and object construction; module 2) spatial navigation and locomotion; module 3) grasping and observation of hand and mouth actions; module 4) action initiation, motor sequences, time encoding; module 5) conditional motor association and learning, action plan switching and action inhibition; module 6) planning defensive actions. These modules can serve as a library of tools to be recombined when faced with novel tasks, and MI might serve as a recombinatory hub. In conclusion, the availability of locally-stored information and multiple outflow paths supports the physiological plausibility of the proposed modular perspective

Grasp-specific motor resonance is influenced by the visibility of the observed actor

Motor resonance is the modulation of M1 corticospinal excitability induced by observation of others' actions. Recent brain imaging studies have revealed that viewing videos of grasping actions led to a differential activation of the ventral premotor cortex depending on whether the entire person is viewed versus only their disembodied hand. Here we used transcranial magnetic stimulation (TMS) to examine motor evoked potentials (MEPs) in the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) during observation of videos or static images in which a whole person or merely the hand was seen reaching and grasping a peanut (precision grip) or an apple (whole hand grasp). Participants were presented with six visual conditions in which visual stimuli (video vs static image), view (whole person vs hand) and grasp (precision grip vs whole hand grasp) were varied in a 2 × 2 × 2 factorial design. Observing videos, but not static images, of a hand grasping different objects resulted in a grasp-specific interaction, such that FDI and ADM MEPs were differentially modulated depending on the type of grasp being observed (precision grip vs whole hand grasp). This interaction was present when observing the hand acting, but not when observing the whole person acting. Additional experiments revealed that these results were unlikely to be due to the relative size of the hand being observed. Our results suggest that observation of videos rather than static images is critical for motor resonance. Importantly, observing the whole person performing the action abolished the grasp-specific effect, which could be due to a variety of PMv inputs converging on M1

Connection between movements of mouth and hand : Perspectives on development and evolution of speech

Mounting evidence shows interaction between manipulative hand movements and movements of tongue, lips and mouth in a vocal and non-vocal context. The current article reviews this evidence and discusses its contribution to perspectives of development and evolution of speech. In particular, the article aims to present novel insight on how processes controlling the two primary grasp components of manipulative hand movements, the precision and power grip, might be systematically connected to motor processes involved in producing certain articulatory gestures. This view assumes that due to these motor overlaps between grasping and articulation, development of these grip types in infancy can facilitate development of specific articulatory gestures. In addition, the hand-mouth connections might have even boosted the evolution of some articulatory gestures. This account also proposes that some semantic sound-symbolic pairings between a speech sound and a referent concept might be partially based on these hand-mouth interactions.Peer reviewe

The left ventral premotor cortex is involved in hand shaping for intransitive gestures: evidence from a two-person imitation experiment

The ventral premotor cortex (PMv) is involved in grasping and object manipulation, while the dorsal premotor cortex (PMd) has been suggested to play a role in reaching and action selection. These areas have also been associated with action imitation, but their relative roles in different types of action imitation are unclear. We examined the role of the left PMv and PMd in meaningful and meaningless action imitation by using repetitive transcranial magnetic stimulation (rTMS). Participants imitated meaningful and meaningless actions performed by a confederate actor while both individuals were motion-tracked. rTMS was applied over the left PMv, left PMd or a vertex control site during action observation or imitation. Digit velocity was significantly greater following stimulation over the PMv during imitation compared with stimulation over the PMv during observation, regardless of action meaning. Similar effects were not observed over the PMd or vertex. In addition, stimulation over the PMv increased finger movement speed in a (non-imitative) finger–thumb opposition task. We suggest that claims regarding the role of the PMv in object-directed hand shaping may stem from the prevalence of object-directed designs in motor control research. Our results indicate that the PMv may have a broader role in ‘target-directed’ hand shaping, whereby different areas of the hand are considered targets to act upon during intransitive gesturing

New insight on the functions organization of the insula of Reil and the inner perisylvian regions: a multidisciplinary approach

The insula of Reil is a wide cortical region (~ 160mm² in rhesus monkey) buried in the depth of the sylvian fissure with an incomplete opercularization in non-human primates that reaches a complete opercularization only in the human brain. Researchers attributed to the insula and adjoining perisylvian regions in both monkeys and humans a very wide range of functions including autonomic and visceral functions, emotions, processing of various sensorial modalities (gustatory, olfactory, somatosensory, auditory). Based on these observations, the present research was undertaken in order to assess the eventual role of the insula and inner perisylvian regions in each of these functions. Two complementary approaches were combined: intracortical microstimulation in awake free behaving monkeys and anatomical connection study. The first study investigates the functional organization of the insula and inner perisylvian regions in macaque monkeys in order to assess a possible somatotopic organization. ICMS experiments were carried out on two awake free-moving rhesus monkeys (macaca mulatta). ICMS was performed with 50 Hz biphasic waves (0.2 msec of phase width) lasting from 50 msec up to 3 sec. Intensity was varied in a range up to 4 mA. During experiments, overt behavior and cardiac activity (ECG) evoked by ICMS have been monitored. The results showed that ICMS of inner perisylvian regions evokes a wide range of behavioral responses, which appeared to be roughly somatotopically arranged. In the rostral part a representation of oro-alimentary behaviour is present; responses like chewing, mouthing and deglutition prevail dorsally (frontal operculum and dorsal insula). In the ventral part (anterior ventral insula), strong viscero-motor responses (vomiting) are evoked. In the middle part (fronto-parietal operculum and middle dorsal insula), complex behaviours are evoked. In the dorsal caudal part (parietal operculum and posterior dorsal insula), simple motor responses involving distal and proximal effectors are evoked. Moreover, in the ventral intermediate sector of the insula, ICMS evoked communicative responses: the stimulations induced the monkey to lip-smack only when facing the experimenter. In the ventral insula and the lower bank, a miscellaneous of stereotyped and repetitive responses was also present. For what concerns the effects of ICMS on the autonomic system, a heart rate variability (HRV) analysis was carried out. The results showed different responses (bradycardia and tachycardia) along the rostro-caudal axis: bradycardia was evoked by stimulation of the rostral portion, showing an increase of the effect along the dorso-ventral axis. The posterior part of the studied regions showed a segregation of spots where stimulation induces bradycardia, tachycardia and no-effect. The present results show the involvement of inner perisylvian regions in the control of behavior as well as in the control of autonomic nervous system functions. Moreover, they show that such control obeys to a coarse somatotopically arranged segregation of functions within the explored regions. In the second experiment, we investigated the cortical and subcortical connections of the insular cortex. Three anatomical tracers were injected in three different sites where the functional properties were studied by mean of ICMS. On the one hand, the findings of this experiment are in agreement with what had been reported in the literature. The anterior insulo-orbital regions where oro-alimentary behaviours were evoked are connected with orbito-frontal areas (area 12, 11, 13 and 14), the rostral ventral prefrontal cortex (area 46), the precentral opercular area (PrCO), anterior cingulate areas (24b\c and 24a, 32), temporal pole, superior temporal pole (STP), inferior temporal gyrus (TEm, TEa\d), entorhinal cortex, baso-lateral amygdaloid nuclei, hypothalamus and ventral tegmental area (VTA). The ventral middle insula, where communicative responses were evoked, shows connections with areas 12r\m, 13l\m and 11 of the orbitofrontal cortex, area 45a of the prefrontal cortex, with area 44, area F5c of the premotor cortex, disgranular opercular area (DO), areas 24c and 24b of the cingulate cortex, temporal pole, TEa and TEm of the inferior temporal cortex, IPa and amygdala. Injection in the most medial part of SII, bordering with the posterior dorsal insula, where simple movement of lower limbs were evoked, is connected with area F3 of the premotor cortex, primary motor cortex, posterior cingulate areas (32, 24d, 23c), primary and secondary somatosensory areas, superior parietal cortex (PE, MIP) and inferior parietal lobule (AIP, PFop, PGop). On the other hand, these findings are in agreement with the functional properties of the injected sites, since the connected areas are functionally involved in different aspects of the behaviours evoked by ICMS performed in the injected loci. Taken together, the findings of these two experiments not only confirm a role of the insular cortex and the inner perisylvian regions in a wide range of behaviours and in the control of the autonomic functions, but also improve our understanding of the dynamics of the involvement of the stimulated regions within neural networks responsible of complex behaviours