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The Lateral Olfactory Tract (Neuropeptide/Glutamate/Aspartate) J

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Proc. Nati. Acad. Sci. USA Vol. 82, pp. 3897-3900, June 1985 Neurobiology N-Acetylaspartylglutamate: Possible role as the neurotransmitter of the lateral olfactory tract (neuropeptide/glutamate/aspartate) J. M. H. FFRENCH-MULLEN*, K. KOLLERt, R. ZACZEKt, J. T. COYLEtt, N. HoRI*, AND D. 0. CARPENTER* *Center for Laboratories and Research, New York State Department of Health, Albany, NY 12201; and tDivision of Child Psychiatry, Departments of Psychiatry and Behavioral Sciences, Pediatrics, Neuroscience and Pharmacology, The Johns Hopkins University School of Medicine, Baltimore, MD 21205 Communicated by Seymour S. Kety, January 2, 1985 ABSTRACT N-Acetylaspartylglutamate, an endogenous from the horse (14) and subsequently from other mammalian brain peptide that binds with high affinity to a subpopulation species (11). Both Ac-Asp and Ac-Asp-Glu are found only in of glutamate-binding sites in rat brain, is excitatory on rat nervous tissue (15-17). A related tripeptide, fB-hydroxy- piriform cortex pyramidal cells studied in a perfused brain butyrylaspartylaspartylglutamate, has been isolated from the slice. Both the monosynaptic excitation of the pyramidal cells spinal cord (18). While the functional roles of these peptides elicited by stimulation of the lateral olfactory tract and the are yet unknown, preliminary reports have indicated that response to N-acetylaspartylglutamate were blocked by DL-2- Ac-Asp-Glu excites cortical neurons and inhibits thalamic amino-4-phosphonobutyrate but not by other excitatory amino and cerebellar neurons in the rat (19), while f-hydroxybu- acid antagonists. Responses to glutamate and aspartate, previ- tyrylaspartylaspartylglutamate is excitatory on cat spinal ously considered to be candidates as the lateral olfactory tract neurons (18). transmitter, were unaffected by 2-amino-4-phosphonobu- Recently Ac-Asp-Glu was found to exhibit a high affinity tyrate. Three days after unilateral bulbectomy there was a for a subset ofbrain receptor sites labeled by L-[3H]glutamate significant decrease in concentrations of N-acetylas- and to produce potent convulsive actions when injected into partylglutamate as well as aspartate, N-acetylaspartate, and rat hippocampus (20). These observations suggest that Ac- y-aminobutyrate in the pyriform cortex of the side from which Asp-Glu could be a transmitter at a site where the receptors the olfactory bulb had been removed. These results are are similar to those for the excitatory amino acids, such as consistent with the possibility that N-acetylaspartylglutamate 'aspartate and glutamate. Consequently we have investigated is the endogenous transmitter of the lateral olfactory tract. the possible actions and pharmacology of Ac-Asp-Glu on rat piriform neurons. The major excitatory input to the olfactory piriform cortex is from fibers of the lateral olfactory tract (LOT) that project METHODS from the olfactory bulb to terminate on the pyramidal neurons. The neurotransmitter released by the LOT termi- Electrophysiology. Tangential piriform cortex slices (300 to nals has been believed to be either aspartate or glutamate. 400 um thick) from Harlan Sprague-Dawley albino rats Both amino acids are excitatory on the pyramidal neurons (150-200 g) were cut by hand, incubated for 1 hr in (1). Electrical stimulation of the LOT results in a calcium- Krebs-Ringer solution, and mounted pial side down for dependent release of aspartate in the rat (2) and glutamate in recording in a chamber, where the slice was totally sub- the guinea pig (3, 4). Removal of the olfactory bulb, which merged and perfused as previously described (8, 9). Bipolar causes a degeneration ofLOT fibers (5), significantly reduces stimulating electrodes were positioned on the LOT. In a few the cortical content ofaspartate and glutamate in both the rat studies the population field potential, reflecting the nearly (2, 5) and guinea pig (6, 7). Furthermore, bulbectomy de- synchronous excitation ofpyramidal neurons by LOT stimu- creases the evoked release of aspartate in the rat (2) and of lation, was examined, and agents that might alter the re- both aspartate and glutamate in the guinea pig (3, 4). sponse were applied by bath perfusion (9). Despite the evidence from these release studies, there is In most studies, single units were recorded extracellularly reason to question the identification of aspartate, glutamate, and identified as pyramidal neurons by demonstrating or both as the transmitter of the LOT fibers. Hori et al. (8, 9) monosynaptic excitation on LOT stimulation. In these stud- observed that DL-2-amino-4-phosphonobutyrate (APB), a ies, transmitter candidates were iontophoretically applied structural analog of glutamate, blocks the LOT-evoked with a constant current source, using one- to three-barrel response but not the responses to iontophoretically applied micropipettes positioned independently of the recording aspartate and glutamate. They concluded that the LOT electrode. The barrels contained Ac-Asp-Glu, Ac-Asp, transmitter is neither aspartate nor glutamate and suggested aspartate, glutamate, and N-methyl-DL-aspartate (Me-Asp) the possibility that the measured release of aspartate and at 10 mM and pH 5.5-7.0 and were applied in a time- glutamate could result from degradation of a peptide rich in controlled sequence (30 sec apart) with ejection currents excitatory amino acids. adjusted to produce responses that were submaximal but as Several compounds derived from aspartate or glutamate equal as possible. Ac-Asp (1 mM) and the excitatory amino in was acid antagonists APB, DL-2-amino-5-phosphonovalerate are present brain tissue. N-Acetylaspartate (Ac-Asp) (APV), glutamate diethyl ester, DL-2-amino-7-phosphono- identified in human brain (10) and subsequently in other and mammalian species (11) and is not a neuronal excitant (12, heptanoate, 'y-D-glutamylglycine, cis-2,3-piperidine 13). N-Acetylaspartylglutamate (Ac-Asp-Glu) was isolated Abbreviations: LOT, lateral olfactory tract; APB, DL-2-amino4 phosphonobutyrate; Ac-Asp, N-acetylaspartate; Ac-Asp-Glu, N- The publication costs of this article were defrayed in part by page charge acetylaspartylglutamate; Me-Asp, N-methyl-DL-aspartate; APV, DL- payment. This article must therefore be hereby marked "advertisement" 2-amino-5-phosphonovalerate; GABA, -aminobutyrate. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 3897 Downloaded by guest on September 29, 2021 3898 Neurobiology: ffrench-Mullen et al. Proc. Natl. Acad. Sci. USA 82 (1985) dicarboxylate, each at 0.1 mM, were bath-perfused for up to Table 1. Effects of antagonists of excitatory amino acids on 20 min, followed by a wash period with control Krebs-Ringer responses to iontophoretically applied Ac-Asp-Glu, solution. Stable and consistent responses were obtained for glutamate, aspartate, and Me-Asp and to a minimum of 10 min; then spikes in five cycles of responses electrically stimulated LOT responses to each agonist were counted and averaged before an an- Depression by antagonist* tagonist was applied. Responses during antagonist perfusions and wash periods were similarly counted and averaged. Stimulation APB GDEE APV APH yDGG PDA Results were expressed as percentages of the control re- LOT 101/105 0/35 0/44 0/15 0/33 0/20 sponse. Ac-Asp-Glu 12/14t 0/5 0/5 0/5 0/5 0/3 Bulbectomy. Male Sprague-Dawley albino rats (150-200 g) Glutamate 0/42t 0/20 4/12 0/9 8/13 0/12 were unilaterally bulbectomized by aspiration of the left Aspartate 0/33t 0/15 9/9§ 4/4§ 2/5 0/5 olfactory bulb while the animals were under chloropenta- Me-Asp 10/44 0/15 11/11§ 4/4§ 3/3§ 0/8 The animals were sacrificed 3 barbital anesthesia (6). days GDEE, glutamate diethyl ester; APH, DL-2-amino-7-phosphono- after surgery, and the brains were removed. Both ipsilateral heptanoate; yDGG, y-D-glutamylglycine; PDA, cis-2-3-piperidine and contralateral piriform cortices were dissected. dicarboxylate. Ac-Asp-Glu, Ac-Asp, and Amino Acid Determinations. *Number of cells depressed by >50%o of the control response/ Dissected tissue was immediately sonicated in 10 vol of number of cells tested. Antagonists were present at 0.1 mM. ice-cold MeOH/H20 (9:1, vol/vol) and centrifuged to pellet tNo significant difference (x2) between Ac-Asp-Glu and LOT APB the precipitated protein. An aliquot of the supernatant was blockade. dried and applied to a Dowex AG 50 column. The lyophilized *p <0.001. eluate was analyzed for Ac-Asp-Glu and Ac-Asp by anion- §Total blockade of cells. exchange high-pressure liquid chromatography as described by Koller et al. (17). An additional aliquot of the deprotein- ated supernatant was allowed to react with o-phthalaldehyde Pharmacology of the Ac-Asp-Glu Response. Previous work in the presence of ethanethiol and analyzed for amino acids has demonstrated that the natural synaptic response of these by reversed-phase high-pressure liquid chromatography and neurons elicited by stimulation ofthe LOT is blocked by APB fluorometric detection (21). (0.1 mM) but not by other antagonists of excitatory amino acids (8, 9). The responses of a pyramidal neuron to Ac-Asp- RESULTS Glu, glutamate, and LOT stimulation are illustrated in Fig. 2. Stimulation of the LOT resulted in either one or two spikes Effects of Ac-Asp-Glu on Piriform Neurons. Ac-Asp-Glu, per stimulus, whereas iontophoretic application of the amino purified to homogeneity from rat brain, was excitatory on all acids and agonists elicited multispiked responses. In this cell 50 neurons examined. The response (Fig. 1) was of short APB (0.1 mM) perfusion for 8.5 min totally blocked both the latency, often starting before the iontophoretic pulse ended. Long iontophoretic ejection times (1-3 sec) with ejection Ac-Asp-Glu and LOT responses, while the glutamate-in- currents up to 100 nA often resulted in spontaneous discharge duced response was unaffected. After a 12-min wash with and loss of spike amplitude, indicative of an excitotoxic control Krebs-Ringer solution the LOT response returned to action.
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  • MR Imaging of Olfactory Bulbs and Tracts

    MR Imaging of Olfactory Bulbs and Tracts

    955 MR Imaging of Olfactory Bulbs and Tracts Masayuki Suzuki1 Olfactory bulbs are easily detected on coronal T1-weighted MR images. They are Tsutomu Takashima situated almost symmetrically opposite either side of the lower end of the olfactory Masumi Kadoya sulci, and, on sagittal images, they are observed as thin soft-tissue bands immediately Shiroh Takahashi beneath the frontal lobe base. On axial images they are shown as oval, paramedian Shiroh Miyayama structures of intermediate intensity. Visualization of the olfactory tract, however, is not always possible. Our study reveals that, on axial images, detection of the olfactory bulb Sakae Taira depends on technical factors; we recommend a 256 x 256 matrix, a 3-mm-thick slice, and less than a 0.6-mm gap. Despite the lack of complete visualization of olfactory bulbs and tracts, MR may be effective in demonstrating diseases of these entities. AJNR 10:955-957, September/October 1989 The radiology literature contains several reports of MR visualization of the cranial nerves [1-3]. However, to our knowledge, there are no reports of the MR appear­ ance of the olfactory nerve. The purpose of this article is to describe the MR appearal}ce of the normal first nerve and to evaluate its detectability on axial MR images. Materials and Methods Sixty-five patients were studied with MR imaging to diagnose suspected intracranial diseases, such as cerebellopontine angle tumor or facial spasm. We used a GE 1.5-T superconductive scanner with a head coil. All images were obtained with a short spin-echo technique of 500/20 (TR/TE), 256 x 128 or 256 x 256 matrices, two or four excitations, 3- mm slice thickness with gaps of 0, 0.3, 0.5, 0.6, 1.0 or 1.5 mm, and fields of view of 12, 16, or 20 em.