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Long-Term Depression of Glutamate-Induced Y-Aminobutyric Proc. Natl. Acad. Sci. USA Vol. 90, pp. 7386-7390, August 1993 Neurobiology Long-term depression of glutamate-induced y-aminobutyric acid release in cerebellum by insulin-like growth factor I (olivo-cerebeilar pathway/neuromodulation/electrical stimulation/microdialysis/pontine nudeus) MANUEL A. CASTRO-ALAMANCOS AND IGNACIO TORRES-ALEMAN Laboratories of Psychobiology and Cellular and Molecular Neuroendocrinology, Cajal Institute, Consejo Superior de Investigaciones Cientificas, Madrid, Spain Communicated by William T. Greenough, April 19, 1993 (received for review November 18, 1992) ABSTRACT We tested the possibility that insulin-like We decided to investigate whether IGF-I might be involved growth factor I (IGF-I) acts as a neuromodulator in the adult in the modulation of neurotransmitter function in the adult cerebellar cortex since previous observations indicated that cerebellar cortex since this area encompasses the climbing IGF-I is located in the olivo-cerebellar system encompassing the fiber terminal fields that synapse onto the dendritic arbors of inferior olive and Purkinje cells. We found that conjoint Purkinje cells. While Purkinje cells use y-aminobutyric acid administration ofIGF-I and glutamate through a microdialysis (GABA) as their main neurotransmitter, they receive a glu- probe stereotaxically implanted into the cerebellar cortex and tamatergic input from projecting granule cells through the deep cerebellar nuclei greatly depressed the release of Y-ami- parallel fiber system. In addition, Purkinje cells receive nobutyric acid (GABA), which normally follows a glutamate another excitatory input from inferior olivary neurons pulse. This inhibition was dose-dependent and long-lasting. through climbing fiber afferents (18). Moreover, the effect was specific for glutamate since KCI- Our working hypothesis was that IGF-I released by inferior induced GABA release was not modified by IGF-I. Basic olive axons would bind to IGF-I receptors in Purkinje cells (3, fibroblast growth factor, another growth-related peptide pres- 9) and modulate their activity. Thus, we first studied whether electrical stimulation of the inferior olive would elicit IGF-I ent in the cerebellum, did not alter the response of GABA to release in the cerebellar cortex. We then explored the effects glutamate stimulation. In addition, electrical stimulation ofthe of exogenous application of IGF-I on the release of GABA in inferior olivary complex significantly raised IGF-I levels in the response to glutamate stimulation in the cerebellum. Finally, cerebellar cortex. Interestingly, when the inferior olive was we determined whether electrical stimulation of the inferior stimulated in conjunction with glutamate administration, olive might modulate the release of GABA induced by GABA release by cerebellar cells in response to subsequent glutamate in a way similar to that seen after exogenous glutamate pulses was depressed in a manner reminiscent ofthat application of IGF-I. seen after IGF-I. These rmdings indicate that IGF-I produces a long-lasting depression of GABA release by Purkinje cells in response to glutamate. IGF-I might be present in climbing fiber MATERIALS AND METHODS terminals and/or cells within the cerebellar cortex and thereby Materials. Recombinant IGF-I and basic fibroblast growth might affect Purkinje cell function. Whether this IGF-I- factor (b-FGF) were purchased from Boehringer Mannheim; induced impairment of glutamate stimulation of Purkinje cells [1251]iodine (2000 Ci/mmol; 1 Ci = 37 GBq) was from New underlies functionally plastic processes such as long-term de- England Nuclear. IGF-I was iodinated to a specific activity pression is open to question. of =2000 Ci/mmol by using the lactoperoxidase method. All other reagents were obtained from Sigma unless otherwise Insulin-like growth factor I (IGF-I) is a trophic and neuro- indicated. modulatory peptide expressed by specific populations of Animals. Wistar rats from our in-house colony were used. neurons in the adult rat brain. Relatively high levels of IGF-I Animals were kept in a 12-h dark/light cycle and received are found in both the developing and the adult cerebellum food and water ad libitum. Animals were handled according At least of the IGF-I content in the adult cerebel- to National Institutes of Health guidelines on animal care. (1-7). part Microdialysis Procedure. Dialysis probes were of concen- lum originates from climbing fiber afferents arising from the tric design using a cuprophan hollow dialysis membrane inferior olivary complex since chemical and surgical lesions sealed at one end with epoxy resin. The other end of the ofthe olivo-cerebellar pathway produce a drastic decrease in membrane was inserted into a 25-gauge stainless steel tube cerebellar IGF-I levels (8). Moreover, the inferior olivary and sealed. A hollow fused silica fiber (140 ,um, o.d.; Poly- complex expresses high levels of IGF-I (9). micro Technologies, Phoenix), which served as the inlet, was In the developing brain, most of the effects of IGF-I on inserted through the length of the 25-gauge stainless steel nerve cells are of a trophic type (10-13) including those on tube to the end of the dialysis membrane. The liquid flows in Purkinje cells in the cerebellar cortex (14). On the other hand, the probe through the fused silica fiber and leaves the fiber at neuromodulatory actions of this peptide in areas such as the the end of the dialysis membrane. hippocampus and the hypothalamus in the adult central Rats were anesthetized with sodium pentobarbital (50 nervous system have been reported by several authors (15, mg/kg, i.p.) and dialysis probes were placed into the cere- 16). Others have shown release of bioactive IGF-I in re- bellar cortex (coordinates: AP = -11.5, L = 2.5; ref. 19) or sponse to neural stimulation (17). These data suggest that into the cerebellar cortex and deep cerebellar nuclei (coor- IGF-I may be a trophic factor during neurogenesis and a dinates: AP = -11.5, L = 2.0, V = 6.5). To dialyze the neuromodulator and/or plasticity mediator in the adult brain cerebeilar cortex, the dialysis membrane extended ventrally (9-14). from the pia 3 mm into the cerebellum. When dialyzing both The publication costs of this article were defrayed in part by page charge Abbreviations: IGF-I, insulin-like growth factor I; GABA, y.ami- payment. This article must therefore be hereby marked "advertisement" nobutyric acid; bFGF, basic fibroblast growth factor; LTD, long- in accordance with 18 U.S.C. §1734 solely to indicate this fact. term depression. 7386 Downloaded by guest on September 25, 2021 Neurobiology: Castro-Alamancos and Torres-Aleman Proc. Natl. Acad. Sci. USA 90 (1993) 7387 the cerebellar cortex and the deep cerebellar nuclei, the dialysis membrane extended from the pia 6.5 mm into the cerebellum. The latter type of probe was used to measure levels of GABA released by Purkinje cells into the deep cerebellar nuclei and at the same time to stimulate Purkinje cell soma and dendrites located in the cerebellar cortex (18). Krebs-Ringer bicarbonate buffer was pumped (syringe pump; Harvard Apparatus) through the dialysis probe at a rate of 2 ,ul/min. After 60-80 min for equilibration, samples were collected every 10 min for the duration of the experi- ment. Four baseline samples followed by infusion of the different test substances for a 40-min period were collected in each experiment. A new baseline period for baseline recov- ery followed and this process was repeated up to three more times. Baseline levels were arbitrarily taken as 100% (see figures). Glutamate pulses were applied at 50 and 5 mM, IGF-I was applied at 100 and 1 nM, bFGF was applied at 100 nM, and KCI was applied at 100 mM. Electrical Stimulation of the Inferior Olive and Pontine Nucleus. After implantation of the dialysis probe in the K cerebellar cortex, a monopolar electrode (0.2 mm diameter; a Rhodes Medical Instruments, Tujunga, CA) was placed into the contralateral inferior olive (AP = -12.5, L = 0.7, V = 9.0) or into the contralateral pontine nucleus (AP = -7.0, L = 1.0; V = 9.5). Placement of the electrode was aided by recording field potentials (P15 Preamplifier; Grass) from the molecular layer with an electrode placed adjacent to the dialysis probe. Monophasic cathodic pulses (3-msec pulse) of 100, 200, and 400 ,uA at a frequency of 5 or 20 Hz were applied for 10 min. Samples for IGF-I determination were collected every 10 min all throughout the procedure. b. ~~~~~4 When inferior olive stimulation was applied in conjunction with glutamate (5 mM), the electrical stimulation lasted 20 FIG. 1. Representative photographs showing the position at min (corresponding to two dialysates of 20 ,ul) and consisted which the microdialysis probe and the microelectrode were placed in of 3-msec pulses at 5 Hz and 300 ILA. the cerebellum (the tract of the probe is indicated by arrowheads) (a) HPLC of GABA. Cerebellar dialysates were analyzed for and in the inferior olive (arrowhead) (b), respectively. GABA content by HPLC (Perkin-Elmer) in a 5-p.m C18 column and a nonlinear gradient with 0.5 M phosphate buffer nucleus, elicited a significant increase in IGF-I levels in the (pH 5.5) and 100o methanol as described by Joseph and dialysate obtained from the cerebellar cortex. The increase Marsden (20). was slightly more effective at 5 Hz as compared to 20 Hz (P IGF-I Radioimmunoassay. The assay procedure has been described in detail (21). Polyclonal rabbit anti-IGF-I (UB3- 189) was a generous gift of The National Pituitary Agency of National Institutes of Health, Chapel Hill (L. Underwood co) 150 and J. Van Wyk). The sensitivity of the assay was 125 pg of 70) IGF-I per ml. Microdialysis samples were directly assayed. Statistics. A one-way analysis of variance followed by a 130 * post-hoc Tukey's test was used when comparing several so Iw groups.
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