scholarly journals Morphological features of large layer V pyramidal neurons in cortical motor-related areas of macaque monkeys: analysis of basal dendrites

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Yu Takata ◽  
Hiroshi Nakagawa ◽  
Taihei Ninomiya ◽  
Hajime Yamanaka ◽  
Masahiko Takada

AbstractIn primates, large layer V pyramidal neurons located in the frontal motor-related areas send a variety of motor commands to the spinal cord, giving rise to the corticospinal tract, for execution of skilled motor behavior. However, little is known about the morphological diversity of such pyramidal neurons among the areas. Here we show that the structure of basal dendrites of the large layer V pyramidal neurons in the dorsal premotor cortex (PMd) is different from those in the other areas, including the primary motor cortex, the supplementary motor area, and the ventral premotor cortex. In the PMd, not only the complexity (arborization) of basal dendrites, i.e., total dendritic length and branching number, was poorly developed, but also the density of dendritic spines was so low, as compared to the other motor-related areas. Regarding the distribution of the three dendritic spine types identified, we found that thin-type (more immature) spines were prominent in the PMd in comparison with stubby- and mushroom-type (more mature) spines, while both thin- and stubby-type spines were in the other areas. The differential morphological features of basal dendrites might reflect distinct patterns of motor information processing within the large layer V pyramidal neurons in individual motor-related areas.

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Taihei Ninomiya ◽  
Ken-ichi Inoue ◽  
Eiji Hoshi ◽  
Masahiko Takada

AbstractThe primate frontal lobe processes diverse motor information in parallel through multiple motor-related areas. For example, the supplementary motor area (SMA) is mainly involved in internally-triggered movements, whereas the premotor cortex (PM) is highly responsible for externally-guided movements. The primary motor cortex (M1) deals with both aspects of movements to execute a single motor behavior. To elucidate how the cortical motor system is structured to process a variety of information, the laminar distribution patterns of signals were examined between SMA and M1, or PM and M1 in macaque monkeys by using dual anterograde tract-tracing. Dense terminal labeling was observed in layers 1 and upper 2/3 of M1 after one tracer injection into SMA, another tracer injection into the dorsal division of PM resulted in prominent labeling in the deeper portion of layer 2/3. Weaker labeling was also visible in layer 5 in both cases. On the other hand, inputs from M1 terminated in both the superficial and the deep layers of SMA and PM. The present data indicate that distinct types of motor information are arranged in M1 in a layer-specific fashion to be orchestrated through a microcircuit within M1.


2020 ◽  
Author(s):  
Edward T Urban ◽  
Mariko Nishibe ◽  
Scott Barbay ◽  
David J Guggenmos ◽  
Randolph J Nudo

AbstractThe rostral forelimb area (RFA) in the rat is considered to be a premotor cortical region based primarily on its efferent projections to the primary motor cortex. The purpose of the present study was to identify corticocortical connections of RFA, and to describe the relative strength of connections with other cortical areas. This will allow us to better understand the broader cortical network in which RFA participates, and thus, determine its function in motor behavior. In the present study, the RFA of adult male Long-Evans rats (n=6) was identified using intracortical microstimulation techniques and injected with the tract tracer, biotinylated dextran amine (BDA). In post-mortem tissue, location of BDA-labeled terminal boutons and neuronal somata were plotted and superimposed on cortical field boundaries. The results demonstrated that the RFA has dense to moderate reciprocal connections with primary motor cortex, the frontal cortex medial and lateral to RFA, primary somatosensory cortex (S1), and lateral somatosensory areas. Importantly, S1 connections were dense to moderate in dysgranular zones, but sparse to negligible in granular zones. Cortical connections of RFA in rat are strikingly similar to cortical connections of the ventral premotor cortex in non-human primates, suggesting that these areas share similar functions.


2019 ◽  
Author(s):  
Jérémy Cousineau ◽  
Léa Lescouzères ◽  
Anne Taupignon ◽  
Lorena Delgado-Zabalza ◽  
Emmanuel Valjent ◽  
...  

AbstractDopamine (DA) plays a crucial role in the control of motor and higher cognitive functions such as learning, working memory and decision making. The primary motor cortex (M1), which is essential for motor control and the acquisition of motor skills, receives dopaminergic inputs in its superficial and deep layers from the midbrain. However, the precise action of DA and DA receptor subtypes on the cortical microcircuits of M1 remains poorly understood. The aim of this work was to investigate how DA, through the activation of D2 receptors (D2R), modulates the cellular and synaptic activity of M1 parvalbumin-expressing interneurons (PVINs) which are crucial to regulate the spike output of pyramidal neurons (PNs). By combining immunofluorescence, ex vivo electrophysiology, pharmacology and optogenetics approaches, we show that D2R activation increases neuronal excitability of PVINs and GABAergic synaptic transmission between PVINs and PNs in layer V of M1. Our data reveal a mechanism through which cortical DA modulates M1 microcircuitry and might participate in the acquisition of motor skills.Significance StatementPrimary motor cortex (M1), which is a region essential for motor control and the acquisition of motor skills, receives dopaminergic inputs from the midbrain. However, precise action of dopamine and its receptor subtypes on specific cell types in M1 remained poorly understood. Here, we demonstrate in M1 that dopamine D2 receptors (D2R) are present in parvalbumin interneurons (PVINs) and their activation increases the excitability of the PVINs, which are crucial to regulate the spike output of pyramidal neurons (PNs). Moreover the activation of the D2R facilitates the GABAergic synaptic transmission of those PVINs on layer V PNs. These results highlight how cortical dopamine modulates the functioning of M1 microcircuit which activity is disturbed in hypo- and hyperdopaminergic states.


PLoS ONE ◽  
2014 ◽  
Vol 9 (1) ◽  
pp. e85109 ◽  
Author(s):  
Michael G. Lacey ◽  
Gerard Gooding-Williams ◽  
Emma J. Prokic ◽  
Naoki Yamawaki ◽  
Stephen D. Hall ◽  
...  

2015 ◽  
Vol 113 (3) ◽  
pp. 937-949 ◽  
Author(s):  
Heather M. Hudson ◽  
Darcy M. Griffin ◽  
Abderraouf Belhaj-Saïf ◽  
Paul D. Cheney

The cortical control of forelimb motor function has been studied extensively, especially in the primate. In contrast, cortical control of the hindlimb has been relatively neglected. This study assessed the output properties of the primary motor cortex (M1) hindlimb representation in terms of the sign, latency, magnitude, and distribution of effects in stimulus-triggered averages (StTAs) of electromyography (EMG) activity recorded from 19 muscles, including hip, knee, ankle, digit, and intrinsic foot muscles, during a push-pull task compared with data reported previously on the forelimb. StTAs (15, 30, and 60 μA at 15 Hz) of EMG activity were computed at 317 putative layer V sites in two rhesus macaques. Poststimulus facilitation (PStF) was distributed equally between distal and proximal muscles, whereas poststimulus suppression (PStS) was more common in distal muscles than proximal muscles (51/49%, respectively, for PStF; 72/28%, respectively, for PStS) at 30 μA. Mean PStF and PStS onset latency generally increased the more distal the joint of a muscle's action. Most significantly, the average magnitude of hindlimb poststimulus effects was considerably weaker than the average magnitude of effects from forelimb M1. In addition, forelimb PStF magnitude increased consistently from proximal to distal joints, whereas hindlimb PStF magnitude was similar at all joints except the intrinsic foot muscles, which had a magnitude of approximately double that of all of the other muscles. The results suggest a greater monosynaptic input to forelimb compared with hindlimb motoneurons, as well as a more direct synaptic linkage for the intrinsic foot muscles compared with the other hindlimb muscles.


2003 ◽  
Vol 89 (6) ◽  
pp. 3205-3214 ◽  
Author(s):  
S. B. Frost ◽  
S. Barbay ◽  
K. M. Friel ◽  
E. J. Plautz ◽  
R. J. Nudo

Although recent neurological research has shed light on the brain's mechanisms of self-repair after stroke, the role that intact tissue plays in recovery is still obscure. To explore these mechanisms further, we used microelectrode stimulation techniques to examine functional remodeling in cerebral cortex after an ischemic infarct in the hand representation of primary motor cortex in five adult squirrel monkeys. Hand preference and the motor skill of both hands were assessed periodically on a pellet retrieval task for 3 mo postinfarct. Initial postinfarct motor impairment of the contralateral hand was evident in each animal, followed by a gradual improvement in performance over 1–3 mo. Intracortical microstimulation mapping at 12 wk after infarct revealed substantial enlargements of the hand representation in a remote cortical area, the ventral premotor cortex. Increases ranged from 7.2 to 53.8% relative to the preinfarct ventral premotor hand area, with a mean increase of 36.0 ± 20.8%. This enlargement was proportional to the amount of hand representation destroyed in primary motor cortex. That is, greater sparing of the M1 hand area resulted in less expansion of the ventral premotor cortex hand area. These results suggest that neurophysiologic reorganization of remote cortical areas occurs in response to cortical injury and that the greater the damage to reciprocal intracortical pathways, the greater the plasticity in intact areas. Reorganization in intact tissue may provide a neural substrate for adaptive motor behavior and play a critical role in postinjury recovery of function.


2021 ◽  
Vol 14 ◽  
Author(s):  
Patricia Perez-García ◽  
Ricardo Pardillo-Díaz ◽  
Noelia Geribaldi-Doldán ◽  
Ricardo Gómez-Oliva ◽  
Samuel Domínguez-García ◽  
...  

Achieving the distinctive complex behaviors of adult mammals requires the development of a great variety of specialized neural circuits. Although the development of these circuits begins during the embryonic stage, they remain immature at birth, requiring a postnatal maturation process to achieve these complex tasks. Understanding how the neuronal membrane properties and circuits change during development is the first step to understand their transition into efficient ones. Thus, using whole cell patch clamp recordings, we have studied the changes in the electrophysiological properties of layer V pyramidal neurons of the rat primary motor cortex during postnatal development. Among all the parameters studied, only the voltage threshold was established at birth and, although some of the changes occurred mainly during the second postnatal week, other properties such as membrane potential, capacitance, duration of the post-hyperpolarization phase or the maximum firing rate were not defined until the beginning of adulthood. Those modifications lead to a decrease in neuronal excitability and to an increase in the working range in young adult neurons, allowing more sensitive and accurate responses. This maturation process, that involves an increase in neuronal size and changes in ionic conductances, seems to be influenced by the neuronal type and by the task that neurons perform as inferred from the comparison with other pyramidal and motor neuron populations.


2020 ◽  
Vol 133 (5) ◽  
pp. 1503-1515 ◽  
Author(s):  
Spyridon Komaitis ◽  
Aristotelis V. Kalyvas ◽  
Georgios P. Skandalakis ◽  
Evangelos Drosos ◽  
Evgenia Lani ◽  
...  

OBJECTIVEThe purpose of this study was to investigate the morphology, connectivity, and correlative anatomy of the longitudinal group of fibers residing in the frontal area, which resemble the anterior extension of the superior longitudinal fasciculus (SLF) and were previously described as the frontal longitudinal system (FLS).METHODSFifteen normal adult formalin-fixed cerebral hemispheres collected from cadavers were studied using the Klingler microdissection technique. Lateral to medial dissections were performed in a stepwise fashion starting from the frontal area and extending to the temporoparietal regions.RESULTSThe FLS was consistently identified as a fiber pathway residing just under the superficial U-fibers of the middle frontal gyrus or middle frontal sulcus (when present) and extending as far as the frontal pole. The authors were able to record two different configurations: one consisting of two distinct, parallel, longitudinal fiber chains (13% of cases), and the other consisting of a single stem of fibers (87% of cases). The fiber chains’ cortical terminations in the frontal and prefrontal area were also traced. More specifically, the FLS was always recorded to terminate in Brodmann areas 6, 46, 45, and 10 (premotor cortex, dorsolateral prefrontal cortex, pars triangularis, and frontal pole, respectively), whereas terminations in Brodmann areas 4 (primary motor cortex), 47 (pars orbitalis), and 9 were also encountered in some specimens. In relation to the SLF system, the FLS represented its anterior continuation in the majority of the hemispheres, whereas in a few cases it was recorded as a completely distinct tract. Interestingly, the FLS comprised shorter fibers that were recorded to interconnect exclusively frontal areas, thus exhibiting different fiber architecture when compared to the long fibers forming the SLF.CONCLUSIONSThe current study provides consistent, focused, and robust evidence on the morphology, architecture, and correlative anatomy of the FLS. This fiber system participates in the axonal connectivity of the prefrontal-premotor cortices and allegedly subserves cognitive-motor functions. Based in the SLF hypersegmentation concept that has been advocated by previous authors, the FLS should be approached as a distinct frontal segment within the superior longitudinal system.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Martje G. Pauly ◽  
Annika Steinmeier ◽  
Christina Bolte ◽  
Feline Hamami ◽  
Elinor Tzvi ◽  
...  

AbstractNon-invasive brain stimulation techniques including repetitive transcranial magnetic stimulation (rTMS), continuous theta-burst stimulation (cTBS), paired associative stimulation (PAS), and transcranial direct current stimulation (tDCS) have been applied over the cerebellum to induce plasticity and gain insights into the interaction of the cerebellum with neo-cortical structures including the motor cortex. We compared the effects of 1 Hz rTMS, cTBS, PAS and tDCS given over the cerebellum on motor cortical excitability and interactions between the cerebellum and dorsal premotor cortex / primary motor cortex in two within subject designs in healthy controls. In experiment 1, rTMS, cTBS, PAS, and tDCS were applied over the cerebellum in 20 healthy subjects. In experiment 2, rTMS and PAS were compared to sham conditions in another group of 20 healthy subjects. In experiment 1, PAS reduced cortical excitability determined by motor evoked potentials (MEP) amplitudes, whereas rTMS increased motor thresholds and facilitated dorsal premotor-motor and cerebellum-motor cortex interactions. TDCS and cTBS had no significant effects. In experiment 2, MEP amplitudes increased after rTMS and motor thresholds following PAS. Analysis of all participants who received rTMS and PAS showed that MEP amplitudes were reduced after PAS and increased following rTMS. rTMS also caused facilitation of dorsal premotor-motor cortex and cerebellum-motor cortex interactions. In summary, cerebellar 1 Hz rTMS and PAS can effectively induce plasticity in cerebello-(premotor)-motor pathways provided larger samples are studied.


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