Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey

doi:10.1016/S0006-8993(71)80001-X

Brain Research

Volume 26, Issue 2, 5 March 1971, Pages 217-233

https://doi.org/10.1016/S0006-8993(71)80001-X Get rights and content

Summary

The intra- and interhemispheric connections of various parts of the precentral gyrus and rostrally adjacent frontal areas are studied with silver impregnation techniques in the rhesus monkey. The subdivisions of the precentral motor area (MI) are found to be connected ipsilaterally in a topographic manner with the premotor area, MII, primary somatosensory area (SI) and the second sensory area (SII). The areas in MI representing the hand and foot do not project to the opposite hemisphere whereas face-, trunk-, and limb-girdle areas do so, and their projections are directed to both homotopical and non-homotopical areas, including topographic projections to MII. These non-homotopical projections form an arch anterior to the projection-free hand and foot areas representing the dorsal aspect of the body from face to occiput and from thoracolumbar to sacral segment of the trunk.

The premotor and arcuate regions can be differentiated on the basis of their intrahemispheric connectivity. The premotor area sends projections to its immediate vicinity (the prefrontal cortex MI and MII), to the superior parietal lobule including the adjacent upper bank of the intraparietal sulcus and to the rostral part of the inferior parietal lobule. In contrast, the projections of areas within the concavity of the arcuate sulcus are directed to the prefrontal cortex, to the caudal part of the inferior parietal lobule including the adjacent lower bank of the intraparietal sulcus and to the cingulate gyrus. Likewise, the interhemispheric connections of the premotor areas and the arcuate areas are mainly found in the homotopic regions except for a small area above the caudal tip of the principal sulcus. The non-homotopic projection of the premotor areas are directed to MI, MII, and prefrontal cortex, whereas those from the arcuate areas are observed in the prefrontal cortex only. The possible significance of these projections is discussed.

References (29)

FinkR.P. et al.
Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system
Brain Research
(1967)
JonesE.G.
Interrelationships of parieto-temporal and frontal cortex in the Rhesus monkey
Brain Research
(1969)
KuypersH.G.J.M. et al.
Occipitotemporal cortico-cortical connections in the rhesus monkey
Exp. Neurol.
(1965)
KuypersH.G.J.M. et al.
Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey
Brain Research
(1970)
MoffettA. et al.
Tactile discrimination performance in the monkey; the effect of ablation of various subdivisions of posterior cortex
Cortex
(1967)
PandyaD.N. et al.
Interhemispheric connections of the precentral motor cortex in the Rhesus monkey
Brain Research
(1969)
PandyaD.N. et al.
Cortico-cortical connections in the Rhesus monkey
Brain Research
(1969)
PandyaD.N. et al.
Interhemispheric projections of the parietal lobe in the Rhesus monkey
Brain Research
(1969)
AstrucJ.
Cortico-cortical efferents from motor and prefrontal cortex in the Rhesus monkey (Macaca mulatta)
Anat. Rec.
(1970)
CurtisH.K.
Intercortical connections of corpus callosum as indicated by evoked potentials
J. Neurophysiol.
(1940)

Denny-BrownD. et al.

The motor functions of the agranular frontal cortex

Res. Publ. Ass. nerv. ment. Dis.

(1948)

Denny-BrownD. et al.

The parietal lobe and behavior

Res. Publ. Ass. nerv. ment. Dis.

(1958)

DevitoJ.L. et al.

Projections from the mesial frontal cortex (supplementary motor area) of the cerebral hemispheres and brain stem of the Macaca mulatta

J. comp. Neurol.

(1959)

EbnerF. et al.

The commissural connections in the neocortex of the monkey

Anat. Rec.

(1962)

Cited by (237)

Homotopic local-global parcellation of the human cerebral cortex from resting-state functional connectivity
2023, NeuroImage
Resting-state fMRI is commonly used to derive brain parcellations, which are widely used for dimensionality reduction and interpreting human neuroscience studies. We previously developed a model that integrates local and global approaches for estimating areal-level cortical parcellations. The resulting local-global parcellations are often referred to as the Schaefer parcellations. However, the lack of homotopic correspondence between left and right Schaefer parcels has limited their use for brain lateralization studies. Here, we extend our previous model to derive homotopic areal-level parcellations. Using resting-fMRI and task-fMRI across diverse scanners, acquisition protocols, preprocessing and demographics, we show that the resulting homotopic parcellations are as homogeneous as the Schaefer parcellations, while being more homogeneous than five publicly available parcellations. Furthermore, weaker correlations between homotopic parcels are associated with greater lateralization in resting network organization, as well as lateralization in language and motor task activation. Finally, the homotopic parcellations agree with the boundaries of a number of cortical areas estimated from histology and visuotopic fMRI, while capturing sub-areal (e.g., somatotopic and visuotopic) features. Overall, these results suggest that the homotopic local-global parcellations represent neurobiologically meaningful subdivisions of the human cerebral cortex and will be a useful resource for future studies. Multi-resolution parcellations estimated from 1479 participants are publicly available (https://github.com/ThomasYeoLab/CBIG/tree/master/stable_projects/brain_parcellation/Yan2023_homotopic).
Sex comparisons of the bilateral deficit in proximal and distal upper body limb muscles
2019, Human Movement Science
Citation Excerpt :
Anatomically, transcallosal fibers connect both hemispheres through the corpus callosum in primates. In addition, the number of transcallosal projections that link proximal muscle representations in the primary somatosensory cortex (S1) and primary motor cortex (M1) areas is larger than those of the distal muscles (Gould, Cusick, Pons, & Kaas, 1986; Pandya & Vignolo, 1971; Rouiller et al., 1994). Thus, the number of corticospinal projections is greater in distal compared to more proximal muscles (Kuypers, 1978; Palmer & Ashby, 1992).
Bilateral deficit (BLD) describes a phenomenon that the force produced during maximal simultaneous bilateral contraction is lower than the sum of those produced unilaterally. The aim of this study was to examine the potential sex-related differences in BLD in upper body proximal and distal limb muscles. Ten men and eight women performed single-joint maximal contractions with their elbow flexors and index finger abductors at separate laboratory visits, during which the maximal isometric voluntary contractions (MVICs) were performed unilaterally and bilaterally with a randomized order in the designated muscle group. Surface electromyographic (EMG) signals were recorded from the prime movers of the designated muscle groups (biceps brachii and first dorsal interosseous) during the maximal contractions. Both men and women demonstrated BLD in their elbow flexors (deficit: men = −11.0 ± 6.3%; women = −10.2 ± 5.0%). Accompanied by this force deficit was the reduced EMG amplitude from the dominant biceps brachii (collapsed across sex: p = 0.045). For the index finger abductors, only men (deficit = −13.7 ± 6.1%), but not women showed BLD. Our results suggested that the BLD in the proximal muscle group is likely induced by the decreased maximal muscle activity from the dominant prime mover. The absence of BLD in women’s index finger muscle is largely due to the inter-subject variability possibly related to the sex hormone flux and unique levels of interhemispheric inhibition.
Motor output, neural states and auditory perception
2019, Neuroscience and Biobehavioral Reviews
Behavior is a complex product of interactions between sensory influx arising from the environment and the neural state of the organism. Therefore, identical sensory input can elicit different behavioral responses. Research in recent years has demonstrated that perception is modulated when an organism is engaged in active behavior – suggesting that neural activity in motor pathways is one factor governing the neural state of networks engaged in sensory processing. In the current manuscript, we focus on the auditory modality and propose a mechanism by which activity in motor cortex changes the neural state in auditory cortex through global inhibition. In turn, such global inhibition reduces auditory net population activity, sharpens auditory frequency tuning curves, shifts the auditory oscillatory state and increases the signal-to-noise ratio of auditory evoked neural activity. These changes can result in either attenuated or enhanced behavioral responses depending on the environmental context. We base our model on animal and human literature and suggest that these motor-induced shifts in sensory states may explain reported phenomena and apparent discrepancies in the literature of motor-sensory interactions, such as sensory attenuation or sensory enhancement.
Distant heterotopic callosal connections to premotor cortex in non-human primates
2017, Neuroscience
Citation Excerpt :
In non-human primates, the majority of brain connectivity data (see datasets established based on the work of Paxinos et al., 2000; Van Essen, 2002; Dubach and Bowden, 2009; Rohlfing et al., 2012; Markov et al., 2014; Calebrese et al., 2015) originate from one hemisphere based on the assumption (though unproven) that lateralization does not play a key role in macaques’. The few available studies (e.g. Pandya and Vignolo, 1971) state that callosal connections predominantly link homotopic cortical regions. This view has been questioned in the past decade (Clarke, 2003) and new evidence of numerous and widespread heterotopic callosal connections have emerged in human studies.
Cortico-cortical connectivity has become a major focus of neuroscience in the last decade but most of the connectivity studies focused on intrahemispheric circuits. Little has been reported about information acquired and processed in the premotor cortex and its functional connection with its homotopic counterpart in the opposite hemisphere via the corpus callosum. In non-human primates (macaques) lateralization is not well documented and its exact role is still unknown. The present study confirms in two macaques the existence of homotopic contralateral projections and completes the picture by further exploring heterotopic (non-motor) callosal projections. This was tested by injecting retrograde tracers in the premotor cortical areas PMv and PMd (targets). Our method consisted of identifying the connections with all the homo- and heterotopic cortical areas located in the contralateral hemisphere. The results showed that PMd and PMv receive multiple low-density labeled inputs from the opposite heterotopic prefrontal, parietal, motor, insular and temporal regions. Such unexpected collection of transcallosal inputs from heterotopic areas suggests that the premotor areas communicate with other modalities through long distance low-density networks which could have important implications in the understanding of sensorimotor and multimodal integration.
Cytoarchitecture and cortical connections of the anterior insula and adjacent frontal motor fields in the rhesus monkey
2015, Brain Research Bulletin
Citation Excerpt :
Like the ventral premotor areas and area ProM, the ventral area 4 receives projections from the rostral part of MII, and from the rostral portion of areas M3 and M4 (orofacial representations). Overall, this projection pattern is in agreement with previous studies which have examined the cortical connections of the ventral precentral orofacial region (e.g., Pandya and Vignolo, 1971; Godschalk et al., 1984; Morecraft et al., 1996; Tokuno et al., 1997) Thus, it seems that, like the dorsal motor proiso- and isocortical areas (Morecraft et al., 2012), the ventral motor proiso- and isocortical areas (area ProM and the ventral portion of area 6) have widespread connections with the prefrontal and parietal cortices as well as with the ventral portions of areas 3, 4, and the rostral portions of MII and the two cingulate motor areas (Fig. 15).
The cytoarchitecture and cortical connections of the ventral motor region are investigated using Nissl, and NeuN staining methods and the fluorescent retrograde tract tracing technique in the rhesus monkey. On the basis of gradual laminar differentiation, it is shown that the ventral motor region stems from the ventral proisocortical area (anterior insula and dorsal Sylvian opercular region). The cytoarchitecture of the ventral motor region is shown to progress in three lines, as we have recently shown for the dorsal motor region. Namely, root (anterior insular and dorsal Sylvian opercular area ProM), belt (ventral premotor cortex) and core (precentral motor cortex) lines. This stepwise architectonic organization is supported by the overall patterns of corticocortical connections. Areas in each line are sequentially interconnected (intralineal connections) and all lines are interconnected (interlinear connections). Moreover, root areas, as well as some of the belt areas of the ventral and dorsal trend are interconnected. The ventral motor region is also connected with the ventral somatosensory areas in a topographic manner. The root and belt areas of ventral motor region are connected with paralimbic, multimodal and prefrontal (outer belt) areas. In contrast, the core area has a comparatively more restricted pattern of corticocortical connections. This architectonic and connectional organization is consistent in part, with the functional organization of the ventral motor region as reported in behavioral and neuroimaging studies which include the mediation of facial expression and emotion, communication, phonic articulation, and language in human.
cTBS delivered to the left somatosensory cortex changes its functional connectivity during rest
2015, NeuroImage
Citation Excerpt :
Outside the shared circuits, sICA showed that cTBS over the SI reduced the degree to which a number of brain regions participate in the four ICs we explored, including in particular a number of brain regions known to be strongly associated with the SI during the planning, execution and observation of motor actions (basal ganglia, cerebellum, BA6 (Rizzolatti et al., 1996)), the processing of tactile stimuli and the observation of touch in others (SII in the parietal operculum, (Keysers et al., 2004)) and the experience and observation of nociceptive stimuli (anterior cingulate, amygdala, (Duerden and Albanese, 2013; Lamm et al., 2011)). Importantly, this network includes regions known to have direct or indirect connections with the region of the SI we have targeted (Jones, 1986; Pandya and Vignolo, 1971; Shanks et al., 1985; Wise et al., 1997). We must stress that not having a functional measurement of the effectiveness of our stimulation limits our conclusions.
The primary somatosensory cortex (SI) plays a critical role in somatosensation as well as in action performance and social cognition. Although the SI has been a major target of experimental and clinical research using non-invasive transcranial magnetic stimulation (TMS), to date information on the effect of TMS over the SI on its resting-state functional connectivity is very scant. Here, we explored whether continuous theta burst stimulation (cTBS), a repetitive TMS protocol, administered over the SI can change the functional connectivity of the brain at rest, as measured using resting-state functional magnetic resonance imaging (rs-fMRI). In a randomized order on two different days we administered active TMS or sham TMS over the left SI. TMS was delivered off-line before scanning by means of cTBS. The target area was selected previously and individually for each subject as the part of the SI activated both when the participant executes and observes actions. Three analytical approaches, both theory driven (partial correlations and seed based whole brain regression) and more data driven (Independent Component Analysis), indicated a reduction in functional connectivity between the stimulated part of the SI and several brain regions functionally associated with the SI including the dorsal premotor cortex, the cerebellum, basal ganglia, and anterior cingulate cortex. These findings highlight the impact of cTBS delivered over the SI on its functional connectivity at rest. Our data may have implications for experimental and therapeutic applications of cTBS over the SI.

View all citing articles on Scopus

^*: A preliminary report of the present findings has been published elsewhere²¹.

^**: Present address: Clinica delle Malattie Nervose e Mentali, Università degli Studi di Trieste, 34129 Trieste, Italy.

View full text

Article preview

Brain Research

Summary

References (29)

Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system

Brain Research

Interrelationships of parieto-temporal and frontal cortex in the Rhesus monkey

Brain Research

Occipitotemporal cortico-cortical connections in the rhesus monkey

Exp. Neurol.

Precentral projections to different parts of the spinal intermediate zone in the rhesus monkey

Brain Research

Tactile discrimination performance in the monkey; the effect of ablation of various subdivisions of posterior cortex

Cortex

Interhemispheric connections of the precentral motor cortex in the Rhesus monkey

Brain Research

Cortico-cortical connections in the Rhesus monkey

Brain Research

Interhemispheric projections of the parietal lobe in the Rhesus monkey

Brain Research

Cortico-cortical efferents from motor and prefrontal cortex in the Rhesus monkey (Macaca mulatta)

Anat. Rec.

Intercortical connections of corpus callosum as indicated by evoked potentials

J. Neurophysiol.

The motor functions of the agranular frontal cortex

Res. Publ. Ass. nerv. ment. Dis.

The parietal lobe and behavior

Res. Publ. Ass. nerv. ment. Dis.

Projections from the mesial frontal cortex (supplementary motor area) of the cerebral hemispheres and brain stem of the Macaca mulatta

J. comp. Neurol.

The commissural connections in the neocortex of the monkey

Anat. Rec.

Cited by (237)

Homotopic local-global parcellation of the human cerebral cortex from resting-state functional connectivity

Sex comparisons of the bilateral deficit in proximal and distal upper body limb muscles

Motor output, neural states and auditory perception

Distant heterotopic callosal connections to premotor cortex in non-human primates

Cytoarchitecture and cortical connections of the anterior insula and adjacent frontal motor fields in the rhesus monkey

cTBS delivered to the left somatosensory cortex changes its functional connectivity during rest

Intra- and interhemispheric projections of the precentral, premotor and arcuate areas in the rhesus monkey*

Summary

Brain Research

Brain Research

Exp. Neurol.

Brain Research

Cortex

Brain Research

Brain Research

Brain Research

Cortico-cortical efferents from motor and prefrontal cortex in the Rhesus monkey (Macaca mulatta)

Anat. Rec.

Intercortical connections of corpus callosum as indicated by evoked potentials

J. Neurophysiol.

The motor functions of the agranular frontal cortex

Res. Publ. Ass. nerv. ment. Dis.

The parietal lobe and behavior

Res. Publ. Ass. nerv. ment. Dis.

Projections from the mesial frontal cortex (supplementary motor area) of the cerebral hemispheres and brain stem of the Macaca mulatta

J. comp. Neurol.

The commissural connections in the neocortex of the monkey

Anat. Rec.