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Two Distinct Inputs to an Avian Song Nucleus Activate Different Glutamate Proc. Natl. Acad. Sci. USA Vol. 88, pp. 4075-4079, May 1991 Neurobiology Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons (N-methyl-D-aspartate/excitatory postsynaptic potentials/birdsong) RICHARD MOONEY AND MASAKAZU KONISHI Division of Biology 216-76, California Institute of Technology, Pasadena, CA 91125 Contributed by Masakazu Konishi, January 23, 1991 ABSTRACT Although neural circuits mediating various might have special significance for the well-known vocal simple behaviors have been delineated, those generating more plasticity exhibited by songbirds. complex behaviors are less well described. The discrete struc- ture of avian song control nuclei promises that circuits con- MATERIALS AND METHODS trolling complex behaviors, such as birdsong, can also be understood. To this end, we developed an in vitro brain slice Brain slices were prepared from 40- to 90-day-old male zebra preparation containing the robust nucleus of the archistriatum finches (Taeniopygia guttata) or Bengalese finches (Lon- (RA), a forebrain song control nucleus, and its inputs from two chura striata) obtained from our breeding colony (all dates other song nuclei, the caudal nucleus of the ventral hyperstri- refer to posthatch age: the hatch day is posthatch 0). Birds atum (HVc) and the lateral part of the magnocellular nucleus were anesthetized with ketamine hydrochloride (0.03-0.06 of the anterior neostriatum (L-MAN). Using intracellular ml), followed by 5-10 min of Metofane (Pitman-Moore, recordings, we examined the pharmacological properties ofthe Washington Crossing, NJ) inhalation, which was discontin- synapses made on RA neurons by L-MAN and HVc axons. ued when the respiratory rate decreased markedly. After a Electrical stimulation of the L-MAN and the HVc fiber tracts second, larger injection of ketamine (0.06-0.09 ml), the bird evoked excitatory postsynaptic potentials (EPSPs) from >70% was decapitated. The brain was removed and placed in of RA neurons when slices were prepared from male birds of ice-cold artificial cerebrospinal fluid (ACSF; see below for 40-90 days ofage, suggesting that many individual RA neurons recipes) that had been equilibrated with 95% 02/5% C02. The brain was blocked transversely about 5 mm rostral of the receive excitatory input from L-MAN and HVc axons. The bifurcation of the midsagittal sinus, and the caudal half of the "L-MAN" EPSPs were blocked by the N-methyl-D-aspartate brain was glued (Loctite, Cleveland) rostral face down to the (NMDA) receptor antagonist D-(-)-2-amino-5-phosphonova- stainless steel tray of the vibratome. Coronal slices were cut leric acid (D-APV) as well as the broad-spectrum glutamate at 400 ,um thickness and transferred to an interface-type receptor antagonist kynurenic acid but were relatively unaf- chamber. The ACSF in the interface chamber was supple- fected by the non-NMDA receptor blocker 6-cyano-7- mented with 0.1% bovine serum albumin (Sigma) and DL- nitroquinoxaline-2,3-dione (CNQX). In contrast, "HVc" EP- (-)-2-amino-5-phosphonovaleric acid (DL-APV) to a final SPs were relatively insensitive to D-APV but almost completely concentration of 100 ,uM. The upper surface of the slice was abolished by CNQX. These experiments suggest that L-MAN exposed to a humidified atmosphere of 95% 02/5% CO2. and HVc axons provide pharmacologically distinct types of After a 1- to 2-hr recovery period, individual brain slices excitatory input to many of the same RA neurons. were transferred to a semisubmersion type recording cham- ber maintained at 35°C, with a perfusion rate of 3-5 ml/min. The differential activation of N-methyl-D-aspartate (NMDA) The fluid level was lowered to within <500 1Lm of the upper and non-NMDA glutamate receptors can produce pro- surface of the slice. ACSF was warmed to 35°C and gassed nounced differences in the output patterns of certain neural with 95% 02/5% CO2 before entering the chamber. Humid- circuits (1-3). We report here that two distinct inputs to the ified 95% 02/5% CO2 was also supplied to the recording same neuron activate primarily NMDA or non-NMDA re- chamber. ceptors in the robust nucleus of the archistriatum (RA), Anatomical reconstruction has shown that L-MAN and which is one ofthe brain areas that controls song in birds. The HVc axons describe different paths to reach RA (personal neural signals for song descend from the caudal part of the observations; see also ref. 8). Although L-MAN and HVc nucleus of the ventral hyperstriatum (HVc) to the RA and fibers travel in roughly parallel dorsoventral trajectories from there to the tracheosyringeal portion ofthe hypoglossal toward RA, L-MAN fibers are displaced laterally to those nucleus (nXIIts), which in turn innervates the vocal muscles arising from HVc. Ultimately, L-MAN axons turn and enter used in singing (4-6). This chain ofnuclei thus constitutes the RA along its lateral face, whereas HVc axons, being more motor pathway for song. The HVc is linked to the RA by medially situated, enter RA along its dorsal edge (see Fig. 1). another series of nuclei, which includes area X, the medial Therefore, coronal slices containing RA were prepared that part of the dorsolateral thalamus, and the lateral part of the allowed the L-MAN and HVc fiber tracts to be electrically magnocellular nucleus of the anterior neostriatum (L-MAN) stimulated independently of one another. Bipolar tungsten (7, 8). This pathway presumably carries auditory information stimulating electrodes were placed <1.0 mm lateral and necessary for the control of song development (9-11). The dorsal to nucleus RA, in areas containing the L-MAN or HVc RA is thus located at the point of convergence between the axon tracts entering the nucleus (see Fig. 1). Electrical vocal motor and auditory pathways. The colocalization of two distinct glutamate receptor subtypes at such a location Abbreviations: NMDA, N-methyl-D-aspartate; EPSP, excitatory postsynaptic potential; RA, robust nucleus of the archistriatum; HVc, caudal nucleus of the ventral hyperstriatum; L-MAN, lateral The publication costs of this article were defrayed in part by page charge part of the magnocellular nucleus of the anterior neostriatum; payment. This article must therefore be hereby marked "advertisement" CNQX, 6-cyano-7-nitroquinoxaline-2,3-dione; ACSF, artificial cere- in accordance with 18 U.S.C. §1734 solely to indicate this fact. brospinal fluid; APV, 2-amino-5-phosphonovaleric acid. 4075 Downloaded by guest on September 27, 2021 4076 Neurobiology: Mooney and Konishi Proc. Natl. Acad. Sci. USA 88 (1991) high divalent ACSF, CaCl2(2H20) and MgSO4(7H20) were 4.0 mM each. For very high divalent ACSF, CaCl2(2H20) and MgSO4(7H20) were 8 mM each. RESULTS The majority of RA neurons responded to L-MAN and HVc fiber stimulation (72 of 98 cells in 30 experiments). Electrical stimulation in the L-MAN and HVc fiber tracts could evoke depolarizing potentials from such "dually innervated" RA neurons (two lower amplitude traces in Fig. 2). Since the depolarizing potentials evoked by stimulating either input by itself could exceed spike threshold, they were classified as excitatory (EPSPs). The "L-MAN" and "HVc" EPSPs recorded from 25 dually innervated RA neurons were ana- lyzed in greater detail. FIG. 1. A schematic of the in vitro finch forebrain slice prepa- A consistent feature of the subthreshold L-MAN and HVc ration shows the placement ofthe intracellular recording electrode in a RA neuron and the location of the extracellular, bipolar stimulating EPSPs was that their shapes differed from each other, as shown electrodes in the L-MAN (lateral) and HVc (dorsal) fiber tracts in Fig. 2. L-MAN EPSPs displayed a shallower onset slope and entering RA. took relatively longer to reach peak amplitude, whereas HVc EPSPs exhibited a steeper onset slope and a substantially stimulation of each fiber tract was accomplished by applying shorter time to peak. In 25 dually innervated RA neurons, the briefvoltages (0.5-20 V), 100 gsec in duration, at a frequency L-MAN EPSP onset slope averaged 1.06 ± 0.13 mV/msec, of 0.1-1 Hz [WPI (New Haven, CT) Pulsemaster], to the significantly less than the value of 1.57 ± 0.14 mV/msec stimulating electrodes. obtained for the HVc EPSP (P < 0.009, n = 25). In the same RA Drugs were delivered to the slice by switching between neurons, the time to peak of the L-MAN response, at 12.28 ± various bathing solutions by means of a solenoid-operated 0.89 msec, was significantly longerthan the value of7.12 ± 0.76 valve assembly (General Valve, Fairfield, NJ). Alternatively, msec measured for the HVc EPSP (P < 0.0001, n = 25). a pressure-driven puffer pipette (WPI PicoPump), prepared L-MAN EPSPs were characterized by a slower initial time from 1-mm capillary glass and drawn to a final tip diameter course than those evoked by HVc fiber stimulation. of 20-50 ,um, was positioned within 400 gm of the recording The interactions between the L-MAN and HVc EPSPs site. Drugs of choice were dissolved in ACSF at known were examined by stimulating the two fiber pathways simul- concentrations and then loaded into the pipette. With this taneously. Since simultaneous stimulation ofthe L-MAN and method, drug concentrations refer to the pipette solution. HVc fiber pathways often drove the cell past spike threshold, The actual bath concentrations were assumed to be substan- the individual stimulus intensities were reduced until the tially lower than the upper limit set by the pipette concen- simultaneous stimulation of the two inputs did not evoke an tration. D-APV and 6-cyano-7-nitroquinoxaline-2,3-dione action potential. The linear sum of the L-MAN and HVc (CNQX) were purchased from Tocris Neuramin (Essex, England).
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