Subthalamic nucleus lesion regularizes firing patterns in globus pallidus and substantia nigra pars reticulata neurons in rats

Subthalamic nucleus lesion altered the statistical properties of the firing patterns of globus pallidus and substantia nigra pars reticulata neurons recorded in urethane anesthetized rats by increasing the proportion of cells in both structures that fired with a very highly regular pattern (from 25%to 50%). In all cases, the most regularly firing neurons fired at a higher mean rate than did more slowly firing neurons. In contrast, globus pallidus lesion shifted the pattern of substantia nigra neurons towards more irregular firing and induced a bursty pattern in two neurons.     

丘脑底核毁损术对帕金森病大鼠脚内核和黑质网状部的影响

目的 :观察毁损丘脑底核 (STN)对帕金森病 (PD)大鼠脚内核 (EP)及黑质网状部 (SNr)γ -氨基丁酸(GABA)能系统的影响。方法 :将 6 0只Wistar大鼠随机分为 6组 ,每组 10只。对照组采用 6 -OHDA立体定向注入大鼠右侧前脑内侧束 (MFB)和中脑被盖腹侧区 (VTA) ,制成偏侧PD模型。实验组分为第Ⅰ、Ⅱ、Ⅲ、Ⅳ和Ⅴ组 ,分别于 6 -OHDA注射前 7d、注射后 1h、2h、3d、7d5个不同时间点 ,局部注射海人藻酸 (KA)破坏STN。 4周后处死大鼠 ,采用免疫组化染色方法 ,定量测量各组大鼠SNr区和EP区的GABA免疫反应阳性区面积和免疫反应强度。实验数据采用方差分析和t检验统计学处理。结果 :GABA免疫组化显示Ⅰ、Ⅱ、Ⅲ、Ⅳ、Ⅴ实验组的注射侧EP面积分别为正常侧的 72 9%、83 7%、79 7%、88 1%、90 1%。对照组注射侧为正常侧面积的 139 1% (P <0 0 5、0 0 1)。各实验组注射侧EP的GABA免疫反应强度 (积分光密度 )均较正常侧减少 ,对照组注射侧较正常侧积分光密度增加 (P <0 0 5 ,P <0 0 1)。Ⅰ、Ⅱ、Ⅲ、Ⅳ、Ⅴ实验组的注射侧SNr面积分别为正常侧的 90 6 %、86 9%、87 3%、80 5 %、80 4%。对照组注射侧面积为正常侧的 10 8 1% (P <0 0 5、0 0 1) ,各实验组注射侧SNr的GABA免疫反应强度均较正常侧减少 ,对照组注射     

Bilateral morphological changes in the substantia nigra of the rat following unilateral damage of the striatum

The effects of damage of the striatum and globus pallidus of one side on the size of cells in the pars reticulata and pars compacta of the substantia nigra on both sides and in the contralateral globus pallidus have been examined. Cellular cross-sectional areas have been compared with those for neurons in the same nuclei in normal age and sex matched littermate control animals. One week after removal of the left striatum and globus pallidus and overlying cortex, the cells in the ipsilateral pars compacta are significantly shrunken (15%). This decrease in size gets progressively more marked with longer survival times reaching 50% 112 days after operation, the longest survival time examined. The shrinkage is accompanied by marked cell loss. Neurons in the contralateral pars compacta show an initial significant hypertrophy of their cell bodies (20%) in the first week after the operation, and later show a shrinkage of 20% at 35 days. The degree of this contralateral shrinkage gradually declines to 12% at 112 days. The changes in the pars compacta are accompanied by a significant enlargement (33%) of the cells in the pars reticulata of the substantia nigra on the side of the damage. This hypertrophy is present by 35 days after operation and persists at least until 112 days. Similar hypertrophy occurs in the ipsilateral globus pallidus in the one case where this could be examined. There are no significant changes in the contralateral pars reticulata, but there is significant enlargement (23%) of the neurons in the contralateral globus pallidus.     

Modulation of dopamine D1-mediated turning behavior and striatal c-fos expression by the substantia nigra

In order to study the possible contribution of the substantia nigra (SN) in the positive interaction between dopamine D₁ receptor agonists and glutamate antagonists in unilaterally 6-hydroxydopamine (6-OHDA) lesioned rats, the effect of the D₁ agonist, SKF 38393, was studied in combination with intranigral infusions of glutamate antagonists of the NMDA (MK 801, CPP) or AMPA (NBQX) type of receptor. Local infusion into the SN of the 6-OHDA lesioned side of MK 801, CPP or NBQX at doses inducing no or minimal behavioral effects significantly increased the turning behavior and the expression of c-fos induced, in the lesioned caudate-putamen (CPu), by a parenteral administration of SKF 38393. The same result was obtained after intra-SN infusion of the GABA agonist, muscimol. High doses of MK 801, CPP or muscimol infused into the SN produced intense contralateral turning per se and induced a sparse c-fos expression in the lesioned CPu which was antagonized by parenteral administration of MK 801. The results indicate that a depression of SN pars reticulata efferent neurons potentiates D₁-mediated responses and suggest that this area may play a role in the positive interaction between glutamate antagonists and D₁ receptor agonists. © 1995 Wiley-Liss, Inc.     

Lesion of the substantia nigra pars compacta downregulates striatal glutamate receptor subunit mRNA expression

This is a study of the effect of the unilateral administration of dopamine (DA) in the pars compacta of the substantia nigra (SN) of the rat on striatal glutamate receptor subunit (GluR1, GluR2 and NMDAR1) gene expression determined by in situ hybridization. The location of the nigral lesion was determined by tyrosine hydroxylase (TH) immunohistochemistry and its extent by the striatal DA and 3,4-dihydroxyphenylacetic acid (DOPAC) concentrations. The DA-induced lesions produce significant bilateral reductions in the expression of GluR1 and NMDAR1 subunit mRNA in the medio-lateral striatum, whereas the expression of striatal GluR2 receptors was not changed. The reduction in GluR1 and NMDAR1 subunit mRNA may be the consequence of glutamatergic hyperactivity developed in the presence of a damaged nigro-striatal system and these may be associated with the genesis of some neurodegenerative diseases.     

丘脑底核电刺激对大鼠黑质网状部及苍白球细胞外神经递质的影响

目的 通过电刺激正常及癫痫大鼠丘脑底核(STN),研究黑质网状部(SNr)及苍白球(GP)细胞外液中谷氨酸(Glu)、γ-氨基丁酸(GABA)的变化,探讨电刺激治疗癫痫的机制.方法 正常大鼠和癫痫大鼠各加只,将刺激电极植入一侧STN,分别用130 Hz和260 Hz进行刺激,同时在同侧的SNr和GP收集细胞外液,用高压液相色谱法检测其Glu和GABA的含量.结果 癫痫大鼠SNr的GABA基础值明显高于正常大鼠.电刺激使两组SNr的GABA明显升高.130 Hz和260 Hz刺激明显增高两组GP和SNr的Glu含量,但130 Hz的更显著.结论 SNr细胞外GABA升高在STN电刺激治疗中起重要作用.电刺激增加了GP细胞的活动,STN电刺激治疗癫痫机制不能单纯解释为"功能的毁损".     

胚胎黑质移植对帕金森病鼠纹状体中多巴胺受体敏感性的影响

大鼠纹状体中多巴胺受体介导的C－fos基因的表达与多巴胺D1受体的超敏现象有关。本实验在鼠胚胎黑质细胞植入帕金森病大鼠模型纹状体后第12周,用免疫组化法检测阿朴吗啡诱发的C－fos蛋白,同时取相邻切片进行酷氨酸羟化酶检测,结果经图像分析发现胚胎黑质移植,能显著减少移植侧纹状体中C－fos的表达量,说明胚胎黑质移植能够纠正多巴胶受体的超敏现象。除此之外,还发现C－fos减少的区域明显超过相邻切片酷氨酸羟化酶免疫阳性区域,表明细胞移植对超敏的多巴胺受体的影响范围大大超过了其诱发宿主残存多巴胺神经元再生的范围。     

Globus pallidus lesions depress the excitatory responses to apomorphine but not amphetamine in the subthalamic nucleus of the behaving rat with a 6-OHDA nigra lesion

The role of the dopaminergic innervation of the basal ganglia on the activity in the subthalamic nucleus (STN) evoked by amphetamine and apomorphine in the behaving rat was examined. The aim was to determine the relationship between that neural activity and the movements evoked by the drugs. Bilateral electrolytic lesions of the globus pallidus (GP), superimposed on the earlier unilateral lesion in substantia nigra (SN) with 6-hydroxydopamine (6-OHDA) affected differently the excitatory responses in the STN evoked by amphetamine and apomorphine and the motor responses to the drugs recorded concurrently. Before the GP lesions, the administration of amphetamine, 5 mg/kg, to the unilaterally deafferented rat induced increased activity in the STN and simultaneously increased movement in the animal. After the GP lesions, the excitatory response to amphetamine in the STN was not different from that seen before the GP lesions. The motor response was also unchanged. In contrast, the GP lesions altered the excitatory response to apomorphine, 3 mg/kg. Before these lesions, the administration of apomorphine to the 6-OHDA lesioned animal evoked a robust and long-lasting excitatory response in the STN and, concurrently, a long-lasting motor response. After the GP lesions, both responses to apomorphine were attenuated. These differential effects of the GP lesions on the unit and motor responses to the two drugs are viewed as representing the effects of the damage in the GP on the dopaminergic innervation contributing to the regulation of activity in the STN. In the 6-OHDA animal, the dopamine afferents innervating the basal ganglia had already been dramatically reduced by 6-OHDA. The GP lesions did not significantly add to the number of these afferents previously eliminated; therefore, the excitatory and motor responses to amphetamine were not changed by the GP lesions. But the GP damage served to eliminate the dopamine receptor in the GP and thus reduced the density of the dopamine receptor in the basal ganglia available for binding to apomorphine. Therefore, the excitatory and motor responses to apomorphine were attenuated after the GP lesions compared to the responses before these lesions.     

Synaptic organization of GABAergic projections from the substantia nigra pars reticulata and the reticular thalamic nucleus to the parafascicular thalamic nucleus in the rat

The ventrolateral part of the parafascicular thalamic nucleus (PF), which is considered to take part in the control mechanism of orofacial motor functions, receives projection fibers not only from the dorsolateral part of the substantia nigra pars reticulata (SNr) but also from the ventral part of the reticular thalamic nucleus (RT) [Tsumori et al., Brain Res. 858 (2000) 429]. In order to better understand the influence of these fibers upon the PF projection neurons, the morphology, synaptology and chemical nature of them were examined in the present study. After ipsilateral injections of Phaseolus vulgaris-leucoagglutinin (PHA-L) into the dorsolateral part of the SNr and biotinylated dextran amine (BDA) into the ventral part of the RT, overlapping distributions of PHA-L-labeled SNr fibers and BDA-labeled RT fibers were seen in the ventrolateral part of the PF. At the electron microscopic level, the SNr terminals made synapses predominantly with the medium to small dendrites and far less frequently with the somata and large dendrites, whereas approximately half of the RT terminals made synapses with the somata and large dendrites and the rest did with the medium to small dendrites of PF neurons. Some of single dendritic as well as single somatic profiles received convergent synaptic inputs from both sets of terminals. These terminals were packed with pleomorphic synaptic vesicles and formed symmetrical synapses. After combined injections of PHA-L into the dorsolateral part of the SNr, BDA into the ventral part of the RT and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) into the ventrolateral part of the striatum or into the rostroventral part of the lateral agranular cortex, WGA-HRP-labeled neurons were embedded in the plexus of PHA-L- and BDA-labeled axon terminals within the ventrolateral part of the PF, where the PHA-L- and/or BDA-labeled terminals were in synaptic contact with single somatic and dendritic profiles of the WGA-HRP-labeled neurons. Furthermore, the SNr and RT axon terminals were revealed to be immunoreactive for gamma-aminobutyric acid (GABA), by using the anterograde BDA tracing technique combined with immunohistochemistry for GABA. The present data suggest that GABAergic SNr and RT fibers may exert different inhibitory influences on the PF neurons for regulating the thalamic outflow from the PF to the cerebral cortex and/or striatum in the control of orofacial movements.     

Monosynaptic and disynaptic projections from the substantia nigra pars reticulata to the parafascicular thalamic nucleus in the rat

We examined a direct pathway and an indirect pathway via the reticular thalamic nucleus (RT) from the substantia nigra pars reticulata (SNr) to the parafascicular thalamic nucleus (PF) by using anterograde and retrograde tract tracing methods. After biotinylated dextranamine (BDA) injection into the dorsolateral part of the SNr, many labeled fibers and axon terminals were distributed in the ventral part of the RT, as well as in the ventrolateral part of the PF, bilaterally with an ipsilateral dominance. After BDA injection into the ventral part of the RT, a plexus of labeled axons was found bilaterally with an ipsilateral dominance in the ventrolateral part of the PF. After combined injections of BDA into the dorsolateral part of the SNr and cholera toxin B subunit (CTb) into the ventrolateral part of the PF on the same side, overlapping distribution of BDA-labeled fibers and CTb-labeled neurons was observed in the ventral part of the RT ipsilateral to the injection sites, where the BDA-labeled axon terminals made symmetrical synaptic contacts with soma and dendrites of the CTb-labeled neurons.     

Substantia nigra pars reticulata lesion induces preconvulsive behavior and changes in glutamate receptor gene expression in the rat brain

The substantia nigra pars reticulata (SNpr) has been proposed to play an important role in the control of the propagation and/or the generation of epileptic seizures. Earlier studies have shown differential effects of the lesion of the SNpr on seizure genesis that demonstrated a regional difference in the anterior and posterior parts of the SNpr in preconvulsive behavior induced by unilateral reticulata injection of dopamine (DA). This study was aimed to investigate some of the underlying mechanisms of the preconvulsive behavior elicited by unilateral SNpr DA injection by the study of changes in the gene expression of glutamate receptor subunits (GluR1, GluR2 and NMDAR1) and of changes in animal behavior following coinfusion of DA and a DA D1 antagonist SCH 23390 into the SNpr. Unilateral injection of exogenous DA into the anterior region of the SNpr induced rapid and short lasting preconvulsive behavior up to wet dog shakes stage and a significant reduction of gene expression for GluR1, GluR2 and NMDAR1 subunits in rat hippocampal subfields including CA1 through CA4 and dentate gyrus (DG) at 1 day after nigral DA injection. The effect was long lasting and persisted for at least 3 weeks. Both preconvulsive behavior and downregulation of glutamate receptor subunit genes were completely blocked by simultaneous coinfusion of DA and SCH 23390. The results suggest, for the first time, that DA D1 receptor in the SNpr may mediate the nigral-involved seizure development. Glutamate desensitization, and/or selective early neuronal damage might be responsible for the downregulation of glutamate receptor subunits by transient preconvulsive activity.     

Expression of ErbB4 in substantia nigra dopamine neurons of monkeys and humans

Abnormal neuregulin-1 signaling through its receptor (ErbB4) might be associated with schizophrenia, although their neuropathological contribution remains controversial. To assess the role of neuregulin-1 in the dopamine hypothesis of schizophrenia, we used in situ hybridization and immunoblotting to investigate the cellular distribution of ErbB4 mRNA in the substantia nigra of Japanese monkeys (Macaca fuscata) and human postmortem brains. In both monkeys and humans, significant signal for ErbB4 mRNA was detected in substantia nigra dopamine neurons, which were identified by melanin deposits. The expression of ErbB4 mRNA in nigral dopamine neurons was confirmed with an independent RNA probe, as well as with combined tyrosine hydroxylase immunostaining. Immunoblotting appeared to support the observation of in situ hybridization. Immunoreactivity for ErbB4 protein was much more enriched in substantia nigra pars compacta containing dopamine neurons than in neighboring substantia nigra pars reticulata. These observations suggest that ErbB4 is expressed in the dopaminergic neurons of primate substantia nigra and ErbB4 abnormality might contribute to the dopaminergic pathology associated with schizophrenia or other brain diseases.     

Movement disorders induced by gamma-aminobutyric agonist and antagonist injections into the internal globus pallidus and substantia nigra pars reticulata of the monkey

Injections of bicuculline into the medial segment of the globus pallidus (GPi) of the monkey induced dose-dependent hypokinesia with dystonic attitudes in contralateral limbs whereas muscimol injections elicited choreiform movements. Injections of the same drugs in substantia nigra pars reticulata (SNr) provoked severe axial postural anomalies with rotational behavior. Conversely, contralateral hypertonia after bicuculline and contralateral hypotonia after muscimol injections were observed. These data suggest that GABA inputs into GPi and SNr play different roles in terms of motor and postural control and add new insights into the pathophysiology of dystonias.     

Reserpine-insensitive dopamine release in the substantia nigra?

Dopamine (DA) is synthesized and released not only from the terminals of the nigrostriatal dopaminergic pathway, but also from the dendrites in the substantia nigra (SN). Whether the DA release in the SN is sensitive to reserpine treatment, as it is in the stratum, has, however, not been clarified. We have determined the effects of reserpine on the concentrations of DA, serotonin and their metabolites in the SN and in the striatum and as an index of DA release in vivo we have assessed the accumulation of the DA metabolite 3-methoxytyramine (3-MT) following inhibition of monoamine oxidase by pargyline. The effects of reserpine on the concentrations of DA and its metabolites were different in the SN as compared to in the striatum. In the striatum there was a maximal depletion of DA to 2% of controls, but in the SN the DA concentration decreased only to 17% of controls. In the SN, the increases of the DA metabolites 3,4-dihydroxyphenylacetic acid (DOPAC) and homovanillic acid (HVA) were less pronounced than in the striatum. In the striatum reserpine treatment (given 15 h, 3.75 h, or 1.75 h before pargyline) decreased the pargyline-induced 3-MT accumulation to 30% of pargyline-treated controls. However, in the SN no effects of reserpine were observed. The results indicate that DA in the SN partly is situated in a reserpine insensitive pool and that the release of DA might be insensitive to reserpine. These differences between the SN and the striatum could be due to different storage mechanisms. In the striatum DA is stored in classical storage granulas but in SN DA is partly stored in storage granulas and partly in smooth endoplasmatic reticulum.     

Parvalbumin and calbindin D-28k in the entopeduncular nucleus,subthalamic nucleus,and substantia nigra of the rat as revealed by double-immunohistochemical methods

The cellular localization of calbindin D-28k (CB) and parvalbumin (PV) was analyzed by means of double-immunohistochemical techniques applied to single sections in the entopeduncular nucleus (EP), the subthalamic nucleus (STh), and the substantia nigra (SN) of the rat. In EP, PV-positive cells abounded centrally, where CB immunostaining was minimal. The medial and ventral sectors of EP were markedly enriched with CB neurophil but devoid of PV-positive cells. CB-positive neurons abounded particularly in the rostral pole of EP. In STh, PV-positive neurons and neuropil were concentrated in the lateral two thirds of this nucleus. Only a few PV-positive cells were detected in sectors of STh devoid of PV-positive neuropil. The STh was completely devoid of CB immunostaining. In the rostral two thirds of SN, PV-positive neurons were largely confined to the lateral half of the pars reticulata (SNR), and occurred more ventrally and medially in the caudal third. Intense CB-immunoreactive neuropil was found in medial and dorsal parts of rostral SNR, and CB-positive cells were observed in the SN pars compacta and the ventral tegmental area. PV and CB cells were also observed in the pars lateralis of SN. The markedly heterogeneous pattern of distribution of PV and CB in EP, STh, and SN suggests that these two calcium-binding proteins may label distinct functional domains in each of these three components of the rat basal ganglia. Synapse 25:359–367, 1997. © 1997 Wiley-Liss, Inc.     

The functional role of the nucleus accumbens in the control of the substantia nigra: Electrophysiological investigations in intact and striatum-globus pallidus lesioned rats

The effects of electrical stimulation of the nucleus accumbens on the activity of identified substantia nigra neurons were studied in intact and lesioned rats. The latter had both the caudate-putamen complex and globus pallidus destroyed by electrolytic lesions. In intact rats a total of 42 of 107 neurons (39.2%) responded to stimulation of the nucleus accumbens. Of the 107 neurons 32 (29.8%) were inhibited and 10 (9.4%) were excited. Pure short inhibitions, long latency inhibitions and excitations followed by inhibition were found in both parts of the substantia nigra. Pure long lasting inhibitions were determined on pars compacta cells only. In lesioned animals, in which the coactivation of striatal and/or cortical fibers traversing the accumbens region was avoided, the percentage of responsive neurons decreased to 20% (23/115). The predominant responses recorded in this situation were pure inhibitions of pars compacta cells (14/46) and long latency inhibitions of pars reticulata neurons (7/69). No pure excitation or excitation-inhibition sequence was recorded. In the two sets of experiments 5 cells were activated antidromically from the nucleus accumbens. The results provide electrophysiological evidence for an inhibitory pathway from the nucleus accumbens to the substantia nigra. The low percentage of responsive neurons, the lack of excitatory responses, the paucity of reciprocal connections and the different inhibitory effects on the two populations of nigral neurons demonstrate that the functional role of the nucleus accumbens in controlling the substantia nigra differs from that exerted by the striatum.     

Excitatory amino acid receptor regulation after subthalamic nucleus lesions in the rat

The subthalamic nucleus plays a pivotal role in the regulation of basal ganglia output. Recent electrophysiologic, lesion and immunocytochemical studies suggest that the subthalamic nucleus uses an excitatory amino acid as a neurotransmitter. After complete ablation of the subthalamic nucleus, we have examined the NMDA, AMPA, kainate and metabotropic subtypes of excitatory amino acid receptors in two major subthalamic projection areas (globus pallidus and substantia nigra pars reticulata) with quantitative autoradiography. Two weeks after ablation, binding sites for [³H]AMPA and [³H]kainate increased in substantia nigra pars reticulata ipsilateral to the lesion. In globus pallidus on the lesioned side, [³H]glutamate binding to the NMDA recognition site decreased. The results suggest that glutamate receptors regulate after interruption of subthalamic nucleus output.     

Regulation of neurotensin-containing neurons in the rat striatum and substantia nigra. Effects of unilateral nigral lesion with 6-hydroxydopamine on neurotensin content and its binding site density

The effect of unilateral lesion of the rat substantia nigra with 6-hydroxydopamine (6-OHDA) was investigated on the endogenous contents of neurotensin (NT) and its binding site densities in the striatum and substantia nigra. Tyrosine hydroxylase (T-OH) activity, γ-aminobutyric acid (GABA) content, binding site densities of dihydrotetrabenazine (TBZOH), a marker of dopaminergic synaptic vesicles, and of iodosulpride, a ligand for dopamine D₂ receptors, were also determined. Fourteen days following nigral lesions, these markers were analyzed by means of radioimmunoassay for NT levels, fluoremetric method for GABA content, radiochemical method for T-OH activity and quantitative autoradiography for NT, TBZOH and iodosulpiride binding site densities. Unilateral nigral lesion with 6-OHDA provoked only ipsilateral modifications in dopamine markers. T-OH activity and TBZOH binding site densities significantly decreased in both the ipsilateral striatum and substantia nigra. Iodosulpiride binding sites decreased in the substantia nigra and increased in the striatum on the ipsilateral side. In contrast to these unilateral changes observed for dopamine markers, dramatic increases in NT contents were found in both the ipsi- and contralateral striata. No change was found in nigral NT levels on either side. On the other hand, NT binding sites decreased in the ipsilateral striatum and substantia nigra, which reflected the destruction of dopaminergic elements in these regions. The present results strongly suggest a dopaminergic control of striatal NT systems and demonstrate that a unilateral loss of this control may lead to strong bilateral alterations in NT levels.     

Ultrastructure of the Gunn rat substantia nigra

Summary The substantia nigra of hyperbilirubinemic (Gunn) rats was studied using light and electron microscopic techniques. PAS-positive inclusions were observed within the neuronal somata of animals 2 to 12 weeks old. Incubation of tissue sections in 0.5% diastase inhibited most of the positive PAS reaction, thus indicating the intraneuronal presence of glycogen.Electron microscopic examination of the tissue substantiated the histochemical data. Mitochondria in neuronal somata contained collections of osmiophilic granules, 200–300 Å diameter, in their intracristal (intermembrane) space. These granules were typical of -glycogen particles.In increasingly older animals (from 2 to 12 weeks old) progressively fewer collections of intramitochondrial glycogen were observed. In these same animals there was, however, a concomitant increase of osmiophilic granules, 400–600 Å diameter, located in the cisternae of granular endoplasmic reticulum. These granules corresponded to -glycogen. After 12 weeks of age, only occasional glycogen granules were seen in either the mitochondria or endoplasmic reticulum.It is suggested that the intramitochondrial glycogen represents an alternate means by which the neuron is able to manufacture ATP following the disruption of oxydative phosphorylation caused by bilirubin. Furthermore it is suggested that with the recovery of oxydative phosphorylation the intramitochondrial collections of glycogen are transferred to the endoplasmic reticulum where glycogenolysis might possibly occur.