Both Supplementary and Presupplementary Motor Areas Are Crucial for the Temporal Organization of Multiple Movements

1998 ◽  
Vol 80 (6) ◽  
pp. 3247-3260 ◽  
Author(s):  
Keisetsu Shima ◽  
Jun Tanji

Shima, Keisetsu and Jun Tanji. Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80: 3247–3260, 1998. To study the involvement of the supplementary (SMA) and presupplementary (pre-SMA) motor areas in performing sequential multiple movements that are individually separated in time, we injected muscimol, a γ-aminobutyric acid agonist, bilaterally into the part of each area that represents the forelimb. Two monkeys were trained to perform three different movements, separated by a waiting time, in four or six different orders. First, each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order, without the visual signals. After the injection of muscimol (3 μl, 5 μg/μl in 10 min) into either the SMA or pre-SMA bilaterally, the animals started making errors in performing the sequence of movements correctly from memory. However, when guided with a visual signal, they could select and perform the three movements correctly. The impaired memory-based sequencing of movements worsened progressively with time until the animals could not perform the task. Yet they still could associate the visual signals with the different movements at that stage. In control experiments on two separate monkeys, we found that injections of the same amount of muscimol into either the SMA or pre-SMA did not cause problems with nonsequential reaching movement regardless of whether it was visually triggered or self-initiated. These results support the view that both the SMA and pre-SMA are crucially involved in sequencing multiple movements over time.

2000 ◽  
Vol 84 (4) ◽  
pp. 2148-2160 ◽  
Author(s):  
Keisetsu Shima ◽  
Jun Tanji

To study how neurons in the medial motor areas participate in performing sequential multiple movements that are individually separated in time, we analyzed neuronal activity in the supplementary (SMA) and presupplementary (pre-SMA) motor areas. Monkeys were trained to perform three different movements separated by waiting times, in four or six different orders. Initially each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order without the visual signals. Three types of neuronal activity were of particular interest; these appeared to be crucially involved in sequencing the multiple motor tasks in different orders. First, we found activity changes that were selective for a particular sequence of the three movements that the monkeys were prepared to perform. The sequence-selective activity ceased when the monkeys initiated the first movement. Second, we found interval-selective activity that appeared in the interval between one particular movement and the next. Third, we found neuronal activity representing the rank order of three movements arranged chronologically; that is, the activity differed selectively in the process of preparing the first, second, or third movements in individual trials. The interval-selective activity was more prevalent in the SMA, whereas the rank-order selective activity was more frequently recorded in the pre-SMA. These results suggest how neurons in the SMA and pre-SMA are involved in sequencing multiple movements over time.


2004 ◽  
Vol 92 (6) ◽  
pp. 3482-3499 ◽  
Author(s):  
Eiji Hoshi ◽  
Jun Tanji

We explored functional differences between the supplementary and presupplementary motor areas (SMA and pre-SMA, respectively) systematically with respect to multiple behavioral factors, ranging from the retrieval and processing of associative visual signals to the planning and execution of target-reaching movement. We analyzed neuronal activity while monkeys performed a behavioral task in which two visual instruction cues were given successively with a delay: one cue instructed the location of the reach target, and the other instructed arm use (right or left). After a second delay, the monkey received a motor-set cue to be prepared to make the reaching movement as instructed. Finally, after a GO signal, it reached for the instructed target with the instructed arm. We found the following apparent differences in activity: 1) neuronal activity preceding the appearance of visual cues was more frequent in the pre-SMA; 2) a majority of pre-SMA neurons, but many fewer SMA neurons, responded to the first or second cue, reflecting what was shown or instructed; 3) in addition, pre-SMA neurons often reflected information combining the instructions in the first and second cues; 4) during the motor-set period, pre-SMA neurons preferentially reflected the location of the target, while SMA neurons mainly reflected which arm to use; and 5) when executing the movement, a majority of SMA neurons increased their activity and were largely selective for the use of either the ipsilateral or contralateral arm. In contrast, the activity of pre-SMA neurons tended to be suppressed. These findings point to the functional specialization of the two areas, with respect to receiving associative cues, information processing, motor behavior planning, and movement execution.


1999 ◽  
Vol 81 (6) ◽  
pp. 3065-3077 ◽  
Author(s):  
Marie-Pierre Deiber ◽  
Manabu Honda ◽  
Vicente Ibañez ◽  
Norihiro Sadato ◽  
Mark Hallett

Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. The human frontomesial cortex reportedly contains at least four cortical areas that are involved in motor control: the anterior supplementary motor area (pre-SMA), the posterior SMA (SMA proper, or SMA), and, in the anterior cingulate cortex, the rostral cingulate zone (RCZ) and the caudal cingulate zone (CCZ). We used functional magnetic resonance imaging (fMRI) to examine the role of each of these mesial motor areas in self-initiated and visually triggered movements. Healthy subjects performed self-initiated movements of the right fingers (self-initiated task, SI). Each movement elicited a visual signal that was recorded. The recorded sequence of visual signals was played back, and the subjects moved the right fingers in response to each signal (visually triggered task, VT). There were two types of movements: repetitive (fixed) or sequential (sequence), performed at two different rates: slow or fast. The four regions of interest (pre-SMA, SMA, RCZ, CCZ) were traced on a high-resolution MRI of each subject’s brain. Descriptive analysis, consisting of individual assessment of significant activation, revealed a bilateral activation in the four mesial structures for all movement conditions, but SI movements were more efficient than VT movements. The more complex and more rapid the movements, the smaller the difference in activation efficiency between the SI and the VT tasks, which indicated an additional processing role of the mesial motor areas involving both the type and rate of movements. Quantitative analysis was performed on the spatial extent of the area activated and the percentage of change in signal amplitude. In the pre-SMA, activation was more extensive for SI than for VT movements, and for fast than for slow movements; the extent of activation was larger in the ipsilateral pre-SMA. In the SMA, the difference was not significant in the extent and magnitude of activation between SI and VT movements, but activation was more extensive for sequential than for fixed movements. In the RCZ and CCZ, both the extent and magnitude of activation were larger for SI than for VT movements. In the CCZ, both indices of activation were also larger for sequential than for fixed movements, and for fast than for slow movements. These data suggest functional specificities of the frontomesial motor areas with respect not only to the mode of movement initiation (self-initiated or externally triggered) but also to the movement type and rate.


2019 ◽  
Author(s):  
Anand Krishnan ◽  
Avehi Singh ◽  
Krishnapriya Tamma

AbstractAnimal color patterns function in varied behavioral contexts including recognition, camouflage and even thermoregulation. The diversity of visual signals may be constrained by various factors, for example, dietary factors, and the composition of ambient environmental light (sensory drive). How have high-contrast and diverse signals evolved within these constraints? In four bird lineages, we present evidence that plumage colors cluster along a line in tetrachromatic color space. Additionally, we present evidence that this line represents complementary colors, which are defined as opposite sides of a line passing through the achromatic point (putatively for higher chromatic contrast). Finally, we present evidence that interspecific color variation over at least some regions of the body is not constrained by phylogenetic relatedness. Thus, we hypothesize that species-specific plumage patterns within these bird lineages evolve by swapping the distributions of a complementary color pair (or dark and light patches in one group, putatively representing an achromatic complementary axis). The relative role of chromatic and achromatic contrasts in discrimination may depend on the environment that each species inhabits.


2009 ◽  
Vol 101 (4) ◽  
pp. 1883-1889 ◽  
Author(s):  
Toshi Nakajima ◽  
Ryosuke Hosaka ◽  
Hajime Mushiake ◽  
Jun Tanji

We attempted to analyze the nature of premovement activity of neurons in medial motor areas [supplementary motor area (SMA) and pre-SMA] from a perspective of coding multiple movements. Monkeys were trained to perform a series of two movements with an intervening delay: supination or pronation with either forearm. Movements were initially instructed with visual signals but had to be remembered thereafter. Although a well-known type of premovement activity representing the forthcoming movements was found in the two areas, we found an unexpected type of activity that represented a second-next movement before initiating the first of the two movements. Typically in the pre-SMA, such activity selective for the second-next movement peaked before the initiation of the first movement, decayed thereafter, and remained low in magnitude while initiating the second movement. This type of activity may tentatively hold information for the second movement while initiating the first. That information may be fed into another group of neurons that themselves build a preparatory activity required to plan the second movements. Alternatively, the activity could serve as a signal to inhibit a premature exertion of the motor command for the second movement.


1973 ◽  
Vol 25 (2) ◽  
pp. 201-206 ◽  
Author(s):  
A. F. Sanders ◽  
A. H. Wertheim

Seven subjects were used in an experiment on the relation between signal modality and the effect of foreperiod duration (EP) on RT. With visual signals the usually reported systematic increase of RT as a function of FP duration (1, 5 and 15 s) was confirmed; with auditory signals no difference was found between FP's of 1 and 5 s while the effect at 15 s was equivalent to that found at 5 s with the visual signal. The results suggest that besides factors such as time uncertainty the FP effect is also largely dependent on the arousing quality of the signal.


2019 ◽  
Vol 10 (1) ◽  
pp. 180-186 ◽  
Author(s):  
Teng Gao ◽  
Yue Liu ◽  
Zifang Zhao ◽  
Yuan Luo ◽  
Lifang Wang ◽  
...  

Abstract Background General anesthesia and increasing age are two main risk factors for postoperative cognitive dysfunction (POCD). Effective agents for the prevention or treatment of POCD are urgently needed. L-655,708, an inverse agonist of α5 subunit-containing γ-aminobutyric acid subtype A (α5GABAA) receptors, can prevent anesthesia-induced memory deficits in young animals. However, there is a lack of evidence of its efficacy in old animals. Methodology Young (3- to 5-month-old) and old (18- to 20-month-old) mice were given an inhalation of 1.33% isoflurane for 1 hour and their associative memory was evaluated 24 hours after anesthesia using fear-conditioning tests (FCTs). To evaluate the effect of L-655,708, mice received intraperitoneal injections of L-655,708 (0.7 mg/kg) or vehicle 30 minutes before anesthesia. Results Old mice exhibited impaired memory and lower hippocampal α5GABAA levels than young mice under physiological conditions. Pre-injections of L-655,708 significantly alleviated isoflurane-induced memory decline in young mice, but not in old mice. Conclusions L-655,708 is not as effective for the prevention of POCD in old mice as it is in young mice. The use of inverse agonists of α5GABAA in preventing POCD in old patients should be carefully considered.


2015 ◽  
Vol 282 (1802) ◽  
pp. 20142284 ◽  
Author(s):  
William L. Allen ◽  
James P. Higham

Careful investigation of the form of animal signals can offer novel insights into their function. Here, we deconstruct the face patterns of a tribe of primates, the guenons (Cercopithecini), and examine the information that is potentially available in the perceptual dimensions of their multicomponent displays. Using standardized colour-calibrated images of guenon faces, we measure variation in appearance both within and between species. Overall face pattern was quantified using the computer vision ‘eigenface’ technique, and eyebrow and nose-spot focal traits were described using computational image segmentation and shape analysis. Discriminant function analyses established whether these perceptual dimensions could be used to reliably classify species identity, individual identity, age and sex, and, if so, identify the dimensions that carry this information. Across the 12 species studied, we found that both overall face pattern and focal trait differences could be used to categorize species and individuals reliably, whereas correct classification of age category and sex was not possible. This pattern makes sense, as guenons often form mixed-species groups in which familiar conspecifics develop complex differentiated social relationships but where the presence of heterospecifics creates hybridization risk. Our approach should be broadly applicable to the investigation of visual signal function across the animal kingdom.


2000 ◽  
Vol 83 (3) ◽  
pp. 1701-1709 ◽  
Author(s):  
Eiichi Naito ◽  
Shigeo Kinomura ◽  
Stefan Geyer ◽  
Ryuta Kawashima ◽  
Per E. Roland ◽  
...  

We examined which motor areas would participate in the coding of a simple opposition of the thumb triggered by auditory, somatosensory and visual signals. We tested which motor areas might be active in response to all three modalities, which motor structures would be activated specifically in response to each modality, and which neural populations would be involved in the speed of the reaction. The subjects were required to press a button with their right thumb as soon as they detected a change in the sensory signal. The regional cerebral blood flow (rCBF) was measured quantitatively with 15O-butanol and positron emission tomography (PET) in nine normal male subjects. Cytoarchitectural areas were delimited in 10 post mortem brains by objective and quantitative methods. The images of the post mortem brains subsequently were transformed into standard anatomic format. One PET scanning for each of the sensory modalities was done. The control condition was rest with the subjects having their eyes closed. The rCBF images were anatomically standardized, and clusters of significant changes in rCBF were identified. These were localized to motor areas delimited on a preliminary basis, such as supplementary motor area (SMA), dorsal premotor zone (PMD), rostral cingulate motor area (CMAr), and within areas delimited by using microstructural i.e., cytoarchitectonic criteria, such as areas 4a, 4p, 3a, 3b, and 1. Fields of activation observed as a main effect for all three modalities were located bilaterally in the SMA, CMAr, contralateral PMD, primary motor (M1), and primary somatosensory cortex (SI). The activation in M1 engaged areas 4a and 4p and expanded into area 6. The activation in SI engaged areas 3b, 1, and extended into somatosensory association areas and the supramarginal gyrus posteriorly. We identified significant activations that were specific for each modality in the respective sensory association cortices, though no modality specific regions were found in the motor areas. Fields in the anterior cingulate cortex, rostral to the CMAr, consistently showed significant negative correlation with mean reaction time (RT) in all three tasks. These results show that simple reaction time tasks activate many subdivisions of the motor cortices. The information from different sensory modalities converge onto the common structures: the contralateral areas 4a, 4p, 3b, 1, the PMD, and bilaterally on the SMA and the CMAr. The anterior cingulate cortex might be a key structure which determine the speed of reaction in simple RT tasks.


Biology Open ◽  
2020 ◽  
Vol 9 (9) ◽  
pp. bio052316
Author(s):  
Anand Krishnan ◽  
Avehi Singh ◽  
Krishnapriya Tamma

ABSTRACTAvian color patterns function in varied behavioral contexts, most being produced by only a handful of mechanisms including feather nanostructures and pigments. Within a clade, colors may not occupy the entire available space, and incorporating complementary colors may increase the contrast and efficacy of visual signals. Here, we describe plumage patterns in four ecologically and phylogenetically diverse bird families to test whether they possess complementary colors. We present evidence that plumage colors in each clade cluster along a line in tetrachromatic color space. Additionally, we present evidence that in three of these clades, this line contains colors on opposite sides of a line passing through the achromatic point (putatively complementary colors, presenting higher chromatic contrast). Finally, interspecific color variation over at least some regions of the body is not constrained by phylogenetic relatedness. By describing plumage patterns in four diverse lineages, we add to the growing body of literature suggesting that the diversity of bird visual signals is constrained. Further, we tentatively hypothesize that in at least some clades possessing bright colors, species-specific plumage patterns may evolve by swapping the distributions of a complementary color pair. Further research on other bird clades may help confirm whether these patterns are general across bird families.


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