Reorganization in motor cortex after brachial plexus avulsion injury and repair with the contralateral C7 root transfer in rats

The purpose of our study was to establish the profile of cortical reorganization in whole BPAI on rats and evaluate changes of cortical reorganization after repair of the median nerve with the contralateral C7 root transfer. Forty adult SD rats underwent whole roots avulsion of left brachial plexus, among them 20 received contralateral C7 root transfer to the injured median nerve. Intracortical microstimulation was performed in primary motor cortex (M1) at intervals of 3, 5, 7, and 10 months, postoperatively. The maps of motor cortical responses were constructed. Five normal rats were used as the control. Results showed that stimulating right M1 elicited motion of left vibrissae, submaxilla, neck, back, and left hindlimb after left BPAI, among them neck representation area replaced the forelimb area throughout the reorganization process. The left forelimb representation area was found in the left motor cortex 5 months after the contralateral C7 root transfer and existed in both motor cortexes at 7th postoperative month. The left forelimb representation area was detected only in right motor cortex at 10th month, postoperatively. In conclusions, after the contralateral C7 root transfer for repair of the median nerve in BPAI, the cortical reorganization occurred in a time‐dependent reorganization. The findings from this study demonstrate that brain involves in the functional recovery after BPAI and repair with nerve transfer and suggest that efforts to improve the results from nerve repair should address the peripheral nerve as well as the brain. © 2010 Wiley‐Liss, Inc. Microsurgery 2010.     

Specific Patterns of Intrinsic Connections between Representation Zones in the Rat Motor Cortex

The organization of intrinsic connections in rat motor cortexwas studied by combining microstimulation and tract-tracingtechniques. Maps of forelimb and vibrissal movements were constructedfrom the distribution of cortical sites from which movementswere evoked in response to intracortical microstimulation. Then,a single injection of a fluorescent dextran was placed intoeither a vibrissal or a wrist representation zone, or into aregion bordering these zones, resulting in anterograde labelingof long intrinsic, horizontal axons. Following injection intothe vibrissal area, axons were largely restricted to the whiskerrepresentation zone and to the border region with the forelimbrepresentation. Injections into a wrist zone labeled projectionslargely restricted to the forelimb area and to the border withthe vibrissal area. Injections into a border region labeleddense projections throughout most of the forelimb and vibrissalareas. These findings indicate that intrinsic axon collateralsin the motor cortex form specific and extensive connectionsamong representation zones related to movements of the samebody part. These connections may be involved in the coordinationof activity in different representation zones for the executionof complex movement patterns. The projection of axon collateralsinto border regions may be the anatomical substrate for therapid reorganization of motor cortical maps that occurs followingvarious experimental manipulations.     

Delayed transplantation with exogenous neurotrophin administration enhances plasticity of corticofugal projections after spinal cord injury

Functional deficits following spinal cord injury (SCI) result from a disruption of corticofugal projections at the lesion site. Not only direct regeneration of the severed axons but also anatomical re-organization of spared corticofugal pathways can reestablish connections between the supraspinal and spinal motor centers. We have previously shown that delayed transplantation of fetal spinal cord tissue and neurotrophin administration by two weeks after SCI supported recovery of forelimb function in adult rats. The current study determined whether the same intervention enhances plasticity of corticofugal fibers at the midbrain and spinal cord level. Anterograde tracing of the left corticorubral fibers revealed that the animals with transplants and neurotrophins (BDNF or NT-3) increased the extent of the traced fibers crossing to the right red nucleus (RN), of which the axons are spared by a right cervical overhemisection lesion. More neurons in the left motor cortex were recruited by the treatment to establish connections with the right RN. The right corticorubral projections also increased the density of midline crossing fibers to the axotomized left RN in response to transplants and neurotrophins. Transplants plus NT-3, but not BDNF, significantly increased the amount of spared corticospinal fibers in the left dorsolateral funiculus at the spinal level both rostral and caudal to the lesion. These results suggest that corticofugal projections retain the capacity until at least two weeks after injury to undergo extensive reorganization along the entire neuraxis in response to transplants and neurotrophins. Targeting anatomical plasticity of corticofugal projections may be a promising strategy to enhance functional recovery following incomplete SCI.     

成年大鼠健侧颈7移位术后跨大脑两半球功能重组的脑电生理研究

目的研究健侧颈7移位至患侧正中神经术后初级运动皮层跨大脑两半球功能重组的时程,初步探讨该重组的中枢机制。方法将45只SD雄性大鼠随机分为9组,即正常对照组(1个组),加左侧全臂丛根性撕脱模型和右侧(健侧)颈7移位模型两组在术后3个月、5个月、7个月、10个月共8个时间组,每组5只。采用运动皮层内微电极电刺激技术,定量评价成年大鼠患肢正中神经代表区在双侧初级运动皮层(初级运动皮层,MI)内的可塑性变化。结果在双侧MI电刺激:(1)正常对照组:一侧肢体的正中神经代表区只在其对侧MI出现。(2)左侧全臂丛根性撕脱模型:在术后3～10个月,患肢的正中神经代表区在双侧MI均能被诱发出来。(3)健侧颈7移位模型:术后3个月,患肢正中神经代表区在双侧MI均未出现。术后5个月,患肢正中神经代表区仅出现于患肢同侧MI。术后7个月,患肢正中神经代表区在双侧MI均出现。术后10个月,患肢正中神经代表区只出现于患肢对侧MI,代表区面积与正常对照无明显差异,且仍位于原前肢代表区。结论在健侧颈7移位成年大鼠模型上证实,在术后10个月初级运动皮层出现了跨大脑两半球的功能重组,并初步探讨了其可能的中枢机制。发现了成年哺乳动物周围神经解剖通路改变后发生跨大脑半球功能重组的脑电生理依据。     

成年大鼠全臂丛根性撕脱伤后初级体感皮层可塑性变化的脑电生理研究

目的 探讨成年大鼠一侧全臂丛根性撕脱伤后双侧初级体感皮层可塑性变化的规律。方法 将30只SD雄性大鼠分为6组，分为正常对照组和全臂丛根性撕脱伤术后1d、7d、1个月、3个月、1年共5个时间组，每组5只。采用体感皮层诱发电位（somatosensory evoked potential，SEP）记录法，定量评价一侧全臂丛根性撕脱伤后双侧初级体感皮层（Sm1）可塑性变化的时程。结果 术后不同时间段电刺激患爪正中神经支配区，在双侧Sm1均未诱发出SEP。电刺激健侧前爪正中神经支配区，在健爪同侧Sm1未记录到SEP，只在其对侧Sm1记录到SEP；但不同时间段的SEP位点数目均明显多于正常对照组。结论 成年大鼠的初级体感皮层仍具有可塑性，一侧全臂丛根性撕脱伤后诱发了双侧Sm1动态的功能重组。两大脑半球相对应的同位区域之间存在着维持半球间平衡和协调的特殊机制。健侧前爪体感代表区的扩大可提高健爪的感觉辨别能力，以部分代偿患肢感觉功能的丧失。     

正中神经损伤修复后大脑运动皮层可塑性变化的实验研究

目的 研究正中神经损伤修复后运动皮层可塑性的变化过程.方法 SD大鼠35只,分为对照组和手术组,手术组又分为术后1 d和1周、4周、8周、12周、16周,每组5只,左侧肢体为损伤修复侧,将正中神经在内侧束分支以远2.0 cm处切断后缝合.通过皮层内微电极刺激技术,定量评价正中神经损伤恢复过程中运动皮层的可塑性变化.结果 正中神经屈指屈腕区运动皮层面积[(0.85±0.1)mm2,-x±s,下同].术后1 d、1周,对侧皮层正中神经屈指屈腕区被桡神经、肌皮神经、腋神经位点占据,没有无反应位点出现;术后4周、8周和16周,运动皮层出现无反应位点;术后8周、12周,对侧皮层出现屈指屈腕位点,差异有统计学意义(P＜0.05);术后16周,与健康组相比,差异无统计学意义(P＞0.05),运动皮层内没有无反应位点出现.结论 成年大鼠正中神经损伤后其对侧运动皮层发生可塑性改变,是一个动态的过程,但其机制还需进一步的研究.     

成年大鼠全臂丛根性撕脱伤后对侧运动皮层可塑性变化的实验研究

目的 探讨成年大鼠全臂丛根性撕脱伤后不同时间段对侧运动皮层的可塑性变化。方法 将30只SD雄性大鼠分为6组，即正常对照组和全臂丛根性撕脱伤术后1d、7d、1个月、3个月、1年共5个时间组，每组5只。采用皮层内微电极电刺激技术，定量评价大鼠左前肢代表区内的可塑性变化。结果 术后不同时间组在原前肢代表区内可诱发出不同的运动类型，包括左侧胡须、下颌、颈部和左下肢4个部位点的运动，但只有颈部位点自始至终占据着术前前肢代表区。结论 成年大鼠的运动皮层仍具有可塑性，术后对侧运动皮层在术前前肢代表区发生了功能重组，并且这种功能重组是动态变化的。瘫痪肢体以上最临近部位的肌肉控制力其代偿性明显增强。     

大鼠健侧颈7移位术后运动皮层兴奋性谷氨酸及其受体变化

目的 探讨大鼠健侧颈7移位术后运动皮层兴奋性谷氨基酸及其受体变化规律.方法 建立颈胸椎后路左侧全臂丛根性撕脱伤和健侧颈7移位正中神经大鼠模型,分别于术后不同时间采用肌电图检测观察正中神经功能的恢复,同时运用运动皮层区微电极刺激法明确大鼠患肢皮层代表区在术后的变化.根据运动皮层区微电极刺激的结果,选择4个皮层重组特异时间点进行取材,行大鼠脑片初级运动皮层区谷氨酸神经元及N-甲基-D-天门冬氨酸受体(NR1、NR2A、NR2B)的免疫组织化学染色.结果 大鼠健侧颈7移位术后,随时间的延长,患侧指深屈肌复合肌肉动作电位潜伏期缩短,波幅升高.术后4个月组,5只大鼠中有3只患爪支配区仅位于同侧运动皮层,同时各手术组双侧运动皮层NR1表达水平均增高,与对照组相比差异有统计学意义(P<0.05).其中右侧运动皮层NR1表达升高显著,与同组对侧相比差异有统计学意义(P<0.05).术后7个月组,4只大鼠患爪支配区位于双侧运动皮层,而且各手术组右侧运动皮层NR2A表达水平升高,与健康大鼠同侧皮层或同组大鼠对侧皮层比较差异均有统计学意义(P<0.05),健侧颈7移位组大鼠右侧皮层NR2A表达水平,较单纯臂丛撕脱或臂丛撕脱健侧颈7切断组同侧皮层升高明显,差异有统计学意义(P<0.05).术后10个月组,3只大鼠患爪支配区位于对侧运动皮层,而在同侧运动皮层却未测到,同时健侧颈7移位组大鼠右侧皮层NR2A表达水平仍维持在升高水平,与其他各组大鼠同侧或同组对侧比较,差异有统计学意义(P<0.05).结论 大鼠全臂丛根性撕脱伤健侧颈7移位正中神经后,大脑发生跨两半球的功能重塑.NR1和NR2A表达的增高可能分别在术后初期和后期功能重组中发挥了一定的作用.     

Repeatedly pairing vagus nerve stimulation with a movement reorganizes primary motor cortex

Although sensory and motor systems support different functions, both systems exhibit experience-dependent cortical plasticity under similar conditions. If mechanisms regulating cortical plasticity are common to sensory and motor cortices, then methods generating plasticity in sensory cortex should be effective in motor cortex. Repeatedly pairing a tone with a brief period of vagus nerve stimulation (VNS) increases the proportion of primary auditory cortex responding to the paired tone (Engineer ND, Riley JR, Seale JD, Vrana WA, Shetake J, Sudanagunta SP, Borland MS, Kilgard MP. 2011. Reversing pathological neural activity using targeted plasticity. Nature. 470:101-104). In this study, we predicted that repeatedly pairing VNS with a specific movement would result in an increased representation of that movement in primary motor cortex. To test this hypothesis, we paired VNS with movements of the distal or proximal forelimb in 2 groups of rats. After 5 days of VNS movement pairing, intracranial microstimulation was used to quantify the organization of primary motor cortex. Larger cortical areas were associated with movements paired with VNS. Rats receiving identical motor training without VNS pairing did not exhibit motor cortex map plasticity. These results suggest that pairing VNS with specific events may act as a general method for increasing cortical representations of those events. VNS movement pairing could provide a new approach for treating disorders associated with abnormal movement representations.     

Partial blocking of NMDA receptors reduces plastic changes induced by short-lasting classical conditioning in the SI barrel cortex of adult mice.

The effect of blockade of N-methyl-D-aspartate (NMDA) receptors in the barrel cortex upon the learning-induced changes of the cortical body map was examined in adult mice. We have previously found that three sensory conditioning sessions, in which stimulation of a row of vibrissae was paired with a tail shock, produced an enlargement of the functional representation of a row of vibrissae stimulated during training. Implantation of the slow release polymer Elvax, containing 2-amino-5-phosphonovalerate (APV, 50 mM), in the vicinity of the barrel cortex was performed 1 day before conditioning to block NMDA receptors. The cortical representation of a trained row of vibrissae was visualized with 2-deoxyglucose (2DG) functional brain mapping 1 day after the completion of the conditioning procedure. The partial blockade of NMDA receptors within the barrel cortex reduced (by half) the expansion of the cortical representation of a trained row of vibrissae as compared to the enlargement of the cortical representation of a trained row found in untreated (60%) and Elvax-PBS implanted (47%) mice. The results provide evidence that the learning-induced processes of cortical map reorganization involve mechanisms that depend on NMDA receptor activation.     

Visualisierung von Phantom- und Rückenschmerzen durch bildgebende Verfahren

If patients with chronic low back pain are stimulated in the painful region, an expanded representation of the back in the primary somatosensory cortex becomes visible that increases with chronicity. This "pain memory" might play an important role in the chronicity process. In patients with phantom limb pain, e.g. subsequent to the amputation of an arm or leg, a shift in the representation of neighboring areas into the deafferented area in primary somatosensory cortex has been observed. This reorganization of functional brain maps is not present in congenital amputees or amputees without phantom limb pain. The magnitude of such pain is positively correlated with this reorganization. We present a model of phantom limb pain that assigns an important role to pre-existing chronic pain. The modulation of plasticity and phantom limb pain by anesthesiological manipulation, the use of NMDA receptor antagonists and opioids is presented. Behaviorally relevant stimulation, e.g. by the use of a myoelectric prosthesis or sensory discrimination training can also influence the cortical somatosensory pain memory. More recent studies focus also on brain areas such as the cingulate gyrus believed to be involved in the affective processing of pain.     

Motor map expansion following repeated cortical and limbic seizures is related to synaptic potentiation.

The effect of experimentally induced seizure activity on the functional reorganization of motor maps has not previously been investigated. Furthermore, while the functional reorganization of motor maps has been thought to involve increases in synaptic communication, there has yet to be a test of this hypothesis. Here we show that repeated seizure activity (kindling), that is accompanied by increased synaptic strength within adult rat motor cortex, results in a doubling of the caudal forelimb motor area. We measured neo-cortical evoked potentials in the right hemisphere prior to 25 days of electrical kindling of the medial frontal corpus callosum or amygdala and re-measured them either 1 or 21 days following the last kindling session. Then, using high resolution intracortical microstimulation (ICMS), the caudal forelimb area in the left hemisphere was mapped. This is the first report of any procedure causing a motor representation to double in size. Furthermore, this expansion was related to the enhanced area of a neocortical polysynaptic field potential and not the motor convulsions per se. Moreover, both the motor map and field potential enhancements were persistent in nature and could be driven from either cortical or limbic sites. The data have implications for human populations with epilepsy.     

Immediate and delayed changes of rat motor cortical output representation with new forelimb configurations.

These experiments examined motor cortical representation patterns after forelimb postural adjustments in rats. The experiments tested the hypothesis that postural adjustments that stretch muscles that are most strongly activated from the primary motor cortex (MI) enlarge their cortical representation. Intracortical electrical stimulation within MI, forelimb muscle activity and movements, and vibrissa movements were used to evaluate the border between the MI forelimb and vibrissa representations before and after forelimb position changes in anesthetized adult rats. The forelimb was originally maintained in retraction (wrist extension and elbow flexion) and then changed to protraction (wrist flexion and elbow extension). Movements and forelimb EMG evoked by electrical stimulation were evaluated during this period (up to 3 hr) through a set of four electrodes implanted in layer V of MI. Changing the forelimb configuration had both immediate and delayed effects on forelimb muscle activity evoked from MI. At some sites, the magnitude of evoked forelimb muscle activity immediately increased with forelimb protraction. At one-quarter of all sites, forelimb muscle activity was evoked where it was not previously detected following an average delay of 22-31 min after forelimb protraction. This change can be interpreted as an expansion of the forelimb area into the vibrissa representation. These data further support the hypothesis that motor cortical representations are flexible and show that sustained changes in somatic sensory input to MI are sufficient to reorganize MI output.     

Thalamic ablations and neocortical development: alterations in thalamic and callosal connectivity.

Corticofugal pathways (callosal, intracortical, and subcortical) have initial axon outgrowth to many areas where no adult connections will persist. Corticofugal projections also demonstrate considerable reorganization after early damage. At the level of gross projections from specific thalamic nuclei to cortical cytoarchitectonic areas, early thalamocortical projections appear to show greater specificity for their targets than do corticofugal projections, and their potential for reorganization after early damage is not known. In this article, we explore the nature of the reorganization shown by the thalamocortical system after early thalamic lesions, and contrast it with reorganization of the origin of contralateral visual callosal projections in the same animals. Hamster pups were given electrolytic lesions in the posterior thalamus on the day of birth, damaging principally either the ventrobasal (somatosensory) or the dorsal lateral geniculate (visual) nucleus. After 30 d of age, HRP was implanted in either the somatosensory or the visual cortex, matching the area of implant with the intended thalamic lesion. The thalamus was reconstructed to determine the remaining nuclei, and the distribution of retrogradely labeled cells was plotted. For animals with HRP implants in visual cortex, the location of callosally projecting cells from the contralateral cortex was charted. These animals were compared to a group of normal adult animals with HRP implants approximately matched for size and location. In seven of eight adult animals with neonatal thalamic lesions, the remaining thalamus did not reorganize to innervate the thalamically denervated cortex. In contrast, the callosal projections from the contralateral visual cortex showed a wider tangential origin in the experimental animals compared to the controls. This expanded callosal projection included cells from temporal cortex, a projection not seen in normal animals. Thus, thalamocortical and callosal projection systems differ in both the magnitude and the nature of their reorganization after early damage.     

Experience-dependent plasticity of the barrel cortex in mice observed with 2-DG brain mapping and c-Fos: effects of MMP-9 KO

Modifications of properties of the adult sensory cortex by elimination of sensory input (deprivation) serves as a model for studying plasticity in the adult brain. We studied the effects of short- and long-term deprivation (sparing one row of vibrissae) upon the barrel cortex. The response to stimulation (exploration of a new environment) of the spared row was examined with [14C]-2-deoxyglucose autoradiography and c-Fos immunohistochemistry. Both methods found large increases of the functional cortical representation of the spared row of vibrissae, extending into parts of the barrel cortex previously activated by the deprived vibrissae. With both methods, the greatest expansion of spared input was observed in cortical layer IV. In this way, we established a model, which was applied for examining involvement of matrix metalloproteinase 9 (MMP-9), upon experience-dependent cortical plasticity. MMP-9 is an enzyme implicated in plastic modification of the neuronal connections. We found that MMP-9 activity was increased in response to stimulation, and furthermore, MMP-9 knockout mice showed a modest but significant decrease of plasticity in layer IV with 2-DG mapping and in layers II/III with c-Fos mapping. Thus, in adult mouse brain experience-dependent plasticity is in part supported by the activity of MMP-9.     

Intrinsic Synaptic Organization of the Motor Cortex

Recent anatomical and electrophysiological studies of the intrinsicsynaptic circuitry of the motor cortex are revealing novel aspectsrelated to the functional organization of this cortical area.These studies demonstrate that the motor cortex is composedof modules consisting of columnar aggregates of neurons relatedto different aspects of the same movement. Excitatory and inhibitoryconnections of intracortical origin link neurons within eachof these cortical modules, and also mediate interactions betweendifferent cortical modules located as far as 2–3 mm fromeach other. The intrinsic excit atory connections utilize glutamate,and act via both NMDA and non-NMDA postsynaptic receptors. Theintrinsic inhibitory connections are GABAergic. Intrinsic corticalcircuits are involved in the temporal coordination of differentcortical modules for the execution of complex movement patterns.In addition, the intrinsic in hibitory and excitatory connectionsare involved in the plasticity of representation zones in themotor cortex, a phenomenon that occurs following nerve damageor during the acquisition of novel motor skills.     

Use-dependent dendritic regrowth is limited after unilateral controlled cortical impact to the forelimb sensorimotor cortex

Compensatory neural plasticity occurs in both hemispheres following unilateral cortical damage incurred by seizures, stroke, and focal lesions. Plasticity is thought to play a role in recovery of function, and is important for the utility of rehabilitation strategies. Such effects have not been well described in models of traumatic brain injury (TBI). We examined changes in immunoreactivity for neural structural and plasticity-relevant proteins in the area surrounding a controlled cortical impact (CCI) to the forelimb sensorimotor cortex (FL-SMC), and in the contralateral homotopic cortex over time (3-28 days). CCI resulted in considerable motor deficits in the forelimb contralateral to injury, and increased reliance on the ipsilateral forelimb. The density of dendritic processes, visualized with immunostaining for microtubule-associated protein-2 (MAP-2), were bilaterally decreased at all time points. Synaptophysin (SYN) immunoreactivity increased transiently in the injured hemisphere, but this reflected an atypical labeling pattern, and it was unchanged in the contralateral hemisphere compared to uninjured controls. The lack of compensatory neuronal structural plasticity in the contralateral homotopic cortex, despite behavioral asymmetries, is in contrast to previous findings in stroke models. In the cortex surrounding the injury (but not the contralateral cortex), decreases in dendrites were accompanied by neurodegeneration, as indicated by Fluoro-Jade B (FJB) staining, and increased expression of the growth-inhibitory protein Nogo-A. These studies indicate that, following unilateral CCI, the cortex undergoes neuronal structural degradation in both hemispheres out to 28 days post-injury, which may be indicative of compromised compensatory plasticity. This is likely to be an important consideration in designing therapeutic strategies aimed at enhancing plasticity following TBI.     

跨突触病毒示踪法研究大鼠C7神经根中枢神经系统支配回路组成

目的 研究假狂犬病病毒减毒株C7神经根注射后标记神经元在脑和脊髓的分布,为健侧C7神经根移位术后的脑功能重塑研究提供实验方法.方法 取SD大鼠20只,根据脊髓和脑组织取材时间随机分为4组:6 h、12 h、24 h和36 h,每组5只动物.在右侧C7神经根注射假狂犬病病毒液2 μl.动物存活6～36 h后,使用抗病毒的多克隆抗体,通过免疫组织化学方法检测相应脊髓节段(C1～C7)和脑中感染的阳性神经元.结果 病毒注射后6～36 h,脊髓和脑中的一些结构及区域可见阳性标记细胞,主要分布在C1～C7节段脊髓灰质、外侧类巨细胞网状核、A5细胞、红核,第一、二运动皮质,第一、二感觉皮质等.随着动物存活时间的延长,脊髓和脑中被标记神经元的数目也明显增多.结论 本跨突触病毒示踪研究发现上述标记的脊髓和脑组织结构与C7神经根存在直接或(和)间接突触联系,可能直接或间接参与对C7神经根的神经支配和调节.     

Cortical connections of functional zones in posterior parietal cortex and frontal cortex motor regions in new world monkeys

We examined the connections of posterior parietal cortex (PPC) with motor/premotor cortex (M1/PM) and other cortical areas. Electrical stimulation (500 ms trains) delivered to microelectrode sites evoked movements of reach, defense, and grasp, from distinct zones in M1/PM and PPC, in squirrel and owl monkeys. Tracer injections into M1/PM reach, defense, and grasp zones showed dense connections with M1/PM hand/forelimb representations. The densest inputs outside of frontal cortex were from PPC zones. M1 zones were additionally connected with somatosensory hand/forelimb representations in areas 3a, 3b, and 1 and the somatosensory areas of the upper bank of the lateral sulcus (S2/PV). Injections into PPC zones showed primarily local connections and the densest inputs outside of PPC originated from M1/PM zones. The PPC reach zone also received dense inputs from cortex caudal to PPC, which likely relayed visual information. In contrast, the PPC grasp zone was densely connected with the hand/forelimb representations of areas 3a, 3b, 1, and S2/PV. Thus, the dorsal parietal-frontal network involved in reaching was preferentially connected to visual cortex, whereas the more ventral network involved in grasping received somatosensory inputs. Additional weak interlinks between dissimilar zones (e.g., PPC reach and PPC grasp) were apparent and may coordinate actions.