Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study

Abstract

Key points The cortical mechanisms of grasping have been extensively studied in macaques and humans; here, we investigated whether common marmosets could rely on similar mechanisms despite strong differences in hand morphology and grip diversity.We recorded electrocorticographic activity over the sensorimotor cortex of two common marmosets during the execution of different grip types, which allowed us to study cortical activity (power spectrum) and physiologically inferred connectivity (phase‐slope index).Analyses were performed in beta (16–35 Hz) and gamma (75–100 Hz) frequency bands and our results showed that beta power varied depending on grip type, whereas gamma power displayed clear epoch‐related modulation.Strength and direction of inter‐area connectivity varied depending on grip type and epoch.These findings suggest that fundamental control mechanisms are conserved across primates and, in future research, marmosets could represent an adequate model to investigate primate brain mechanisms. AbstractThe cortical mechanisms of grasping have been extensively studied in macaques and humans. Here, we investigated whether common marmosets could rely on similar mechanisms despite striking differences in manual dexterity. Two common marmosets were trained to grasp‐and‐pull three objects eliciting different hand configurations: whole‐hand, finger and scissor grips. The animals were then chronically implanted with 64‐channel electrocorticogram arrays positioned over the left premotor, primary motor and somatosensory cortex. Power spectra, reflecting predominantly cortical activity, and phase‐slope index, reflecting the direction of information flux, were studied in beta (16–35 Hz) and gamma (75–100 Hz) bands. Differences related to grip type, epoch (reach, grasp) and cortical area were statistically assessed. Results showed that whole‐hand and scissor grips triggered stronger beta desynchronization than finger grip. Task epochs clearly modulated gamma power, especially for finger and scissor grips. Considering effective connectivity, finger and scissor grips evoked stronger outflow from primary motor to premotor cortex, whereas whole‐hand grip displayed the opposite pattern. These findings suggest that fundamental control mechanisms, relying on adjustments of cortical activity and connectivity, are conserved across primates. Consistently, marmosets could represent a good model to investigate primate brain mechanisms.

Data-driven Koopman operator approach for computational neuroscience

“…3) in the hierarchy of modes retrieved by Koopman analysis; specifically, they correspond to the complex-conjugate pairs {z 5 , z 6 }, {z 9 , z 10 }, and {z 13 , z 14 } (henceforth abbreviated z 5,6 , z 9,10 , and z 13,14 , respectively). These response frequencies correspond to the Beta band in several primate species including the marmoset [8,37,61]. Our result thus confirms prior studies that find a change in Beta frequency associated with sound deviants or natural dynamically modulated sounds [8,37].…”

“…As per [61], we expected the spatiotemporal dynamics of the reconstructed signal for z 141,142 to be localized. That is, a plot of the signal displayed over the electrodes matrix should exhibit more diversity in space than slower frequencies (e.g., Beta shown in Fig.…”

Whole brain mapping of somatosensory responses in awake marmosets investigated with ultra-high field fMRI

“…electrophysiological recordings, calcium imaging, optogenetics). This whole brain mapping can be performed for a more detailed body representation and combined to other sensory modalities (visual, auditory) to explore multisensory integration process (Cléry et al, 2015(Cléry et al, , 2017b(Cléry et al, , 2020, or to functional tasks to explore motor-related function such as grasping (Tia et al, 2017). auditory anterolateral area; AuCl, auditory caudaolateral area; AuCPB, auditory caudal parabelt area; AuML, auditory middle lateral area; AuRT, auditory rostrotemporal area; AuR, auditory rostral area; FST, fundus of the superior temporal sulcus; IPa, intraparietal sulcus associated area;…”

Prehensile kinematics of the marmoset monkey: Implications for the evolution of visually‐guided behaviors

“…Typically, the configuration of the hand is scaled according to the intrinsic properties of the object such as its shape and size, while a faster velocity is observed when reaching for larger objects, as greater precision is required for smaller targets. While these traits are well characterized in primates that adopt a precision grip, it is unknown if this would be similar in marmosets, who do not possess opposable digits and use variants of power and scissor grips for prehension (Tia et al, ). One exception is the New World Capuchin monkey that can perform a functional precision grip using pseudo‐opposable thumbs (Bishop, ; Christel & Fragaszy, ).…”

“…Furthermore, their brain architecture has been extensively mapped (Paxinos, Watson, Petrides, Rosa, & Tokuno, ) and is highly comparable to humans (Chaplin, Yu, Soares, Gattass, & Rosa, ), sharing many analogous areas especially in the visual system that enables remarkable visual perception and acuity (Mitchell & Leopold, ). Little work, however, has evaluated the prehensile capacity of these animals (Hashimoto, Yamazaki, & Iriki, ; Tia et al, ; Yumiko Yamazaki et al, ) which is important from a teleological and evolutionary perspective as well as for providing the framework upon which appropriate studies can be designed around their limitations. From a logistical perspective, marmosets have been considered notoriously difficult to train, exhibiting a lower yield in trials per session due to their lower attentional span (Range & Huber, ) and greater reliance on social company (Burkart, Fehr, Efferson, & Van Schaik, ).…”