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C-Fos Expression in the Pons and Medulla of the Cat During Carbachol-Induced Active Sleep

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C-Fos Expression in the Pons and Medulla of the Cat During Carbachol-Induced Active Sleep The Journal of Neurosdence. June 1993. 136): 2703-2716 C-fos Expression in the Pons and Medulla of the Cat during Carbachol-induced Active Sleep J. Yamuy, J. R. Mantillas, F. Ft. Morales, and M. H. Chase Department of Physiology, Department of Anatomy and Cell Biology, and the Brain Research Institute, University of California, Los Angeles, California 90024 Microinjection of carbachol into the rostra1 pontine tegmen- beenshown that a state comparable to active sleepcan be elicited turn of the cat induces a state that is comparable to naturally by the microinjection of cholinergic agonists,such ascarbachol, occurring active (REM, rapid eye movement) sleep. We sought into the rostra1pontine tegmentum of chronic cats. The evoked to determine, during this pharmacologically induced behav- state resemblesactive sleep by behavioral, polygraphic, and ioral state, which we refer to as active sleep-carbachol, the electrophysiologic criteria (George et al., 1964; Baghdoyan et distribution of activated neurons within the pons and medulla al., 1987, 1989; Morales et al., 1987); it can also be reliably and using c-fos immunocytochemistry as a functional marker. repeatedly induced. Thus, it offers significant methodological Compared with control cats, which were injected with sa- advantages in terms of an experimental paradigm to study the line,‘active sleep-carbachol cats exhibited higher numbers state-dependentactivity of CNS neurons. of c-fos-expressing neurons in (1) the medial and portions Furthermore, at a cellular level of analysis, several lines of of the lateral reticular formation of the pons and medulla, (2) evidence indicate that neurons that are located in certain struc- nuclei in the dorsolateral rostra1 pons, (3) various raphe nu- tures of the rostra1 pontine tegmentum and in the medullary clei, including the dorsal, central superior, magnus, pallidus, reticular formation are involved in the generation and main- and obscurus, (4) the medial and lateral vestibular, prepos- tenance of active sleep (Siegel, 1989; Steriade and McCarley, itus hypoglossi, and intercalatus nuclei, and (5) the abdu- 1990; Jones, 1991). Nonetheless, the specific sets of neurons tens nuclei. On the other hand, the mean number of c-fos- within the pons and medulla that are responsiblefor this be- expressing neurons found in the masseter, facial, and hy- havioral state have not been clearly demarcated. A major dif- poglossal nuclei was lower in carbachol-injected than in con- ficulty has been in relating the activity of identified population trol cats. of neurons to the behavioral state of the animal and to specific The data indicate that c-fos expression can be employed physiological processes;this problem reflects, in part, the lim- as a marker of state-dependent neuronal activity. The spe- itations of the methodologies that have been employed. For cific sites in which there were greater numbers of c-fos- example, with electrophysiological recording techniques, only a expressing neurons during active sleep-carbachol are dis- fraction of the neuronal populations in a given area can be cussed in relation to the state of active sleep, as well as the sampled. On the other hand, whereas a large number of cells functional role that these sites play in generating the various can be examined employing classical anatomical and neuro- physiological patterns of activity that occur during this state. chemical procedures,the data lack the necessaryfunctional cor- [Key words: active sleep, atonia, carbachol, c-fos expres- relates. Problems such as these indicate the need to incorporate sion, Fos protein, immunocytochemistry] new techniques that can assess,during active sleep, the func- tional state of large populations of anatomically identified neu- Active sleepis a state present in mammals characterized poly- rons. graphically by a desynchronized EEG activity, muscularatonia, Recently, the expressionof the proto-oncogene c-fos hasbeen high-amplitude bioelectrical waves in the pons, lateral genicu- related to certain forms of neuronal activation (Hunt et al., 1987; late nuclei, and occipital cortex called ponto-geniculo-occipital Sagaret al., 1988; Menttrey et al., 1989; for review, seeMorgan (PGO) waves, and rapid eye movements (for recent reviews, see and Curran, 199I). The expression of this genecan be detected Siegel, 1989; Steriade and McCarley, 1990;Jones, 1991). A great with single-cellresolution by the nuclear localization of its pro- deal of fundamental information has been obtained regarding tein product (Fos) using immunocytochemical techniques(Hunt the physiology, pharmacology, and anatomical location of neu- et al., 1987). However, there are a number of factors that must ronal populations implicated in active sleep(which is also called be taken into account when dealing with an analysis of the in paradoxical, REM, and desynchronizedsleep; Siegel, 1989; Ster- vivo expressionof c-fos. A carefully designedexperimental pro- iade and McCarley, 1990; Jones, 1991). For example, it has tocol and strict control experiments are required in order to optimize and set a baseline of c-fos expression. In addition, there are potential problems in interpreting the results of such Received June 19, 1992; revised Nov. 27, 1992; accepted Dec. 3, 1992. studies(see Dragunow and Faull, 1989). Nevertheless,by taking We are grateful to Mrs. Sharon Sampogtta for her excellent histological work and Robert Tran for his technical assistance. We thank Dr. Dennis Slamon for the precedinginto account, we believe that it is possibleto obtain his generous contribution of the antibody to Fos. This work was supported by an anatomical correlate of neuronal activation that occurs dur- U.S. Public Health Service Grants AG04307, NS09999, and MH43362. ing a behavioral state by mapping the cellular expression of Correspondence should be addressed to Jack Yamuy, Department ofPhysiology, UCLA School of Medicine, Los Angeles, CA 90024. c-fos. Copyright Q 1993 Society for Neuroscience 0270-6474/93/132703-16$05.00/O In the present study, we tested the hypothesis that the neu- 2704 Yamuy et al. * C-fos Expression during Carbachol-induced Active Sleep ronal populations activated during the carbachol-induced state, the alkaline phosphatase method, and in 2% normal goat serum (NGS) with 0.3% Triton X in Tris-buffered saline (TBS; pH 7.4) in the case of which has been used as a model of naturally occurring active sections that were immunostained using the avidin-biotin procedure sleep, can be detected using c-fos immunocytochemistry. Our (Hsu et al., I98 I). In all cases, sections were incubated overnight in a results show that in carbachol-injected cats, neurons located in rabbit polyclonal Fos antiserum raised against an in vitro-translated pontine and medullary regions that have been previously im- gene product. Incubations were carried out overnight at room temper- plicated in active sleep exhibit c-fos immunoreactivity. In ad- ature in a humilied chamhr in a primary antibody dilution of I : 10,000. Control slides were similarly incubated in a blocking or NGS solution. dition, it was observed that other regions contained c-fos-ex- Fos immunoreactivity was visualized by the alkaline phosphatax pressing neurons, which suggeststhat they are involved in method using an anti-rabbit alkaline phosphatase-conjugated secondary mediating the various patterns of physiological activity that are antibody (Promega Corp., Madison, WI) and by the avidin-biotin pro- presentduring this state. cedure using the anti-rabbit ABC “Elite” kit (Vector Laboratories, Bur- lingame, CA). In the former case, slides were rinsed in TBST (Tris- Preliminary resultsofthis work have beenpreviously reported buffered saline, pH 8,0.05% Tween 20) and incubated for 3 hr at room Yamuy et al., 1991). temperature in the anti-rabbit InG alkaline Dhosphatase coniuaate at a diluiion of I : 1000. After rinsing in TBST, they were reacted-wqth Pro- mesa NTB (6.6 ul/ml)-BCIP (3.3 ul/ml1 in TBS (DH 9.5) for 30-60 min. Materials and Methods The reactioh was stopped by‘rekated’rinsing $th ED?‘A/TBS (pH 8) Experiments were performed on five adult cats. for 45-60 min. During this step the slides were kept in a darkened Surgical procedures. The following surgicalprocedures were per- environment. After processing, a coverslip was added using 2: I glycerin- formed under sodiumnentobarbital anesthesia (40 mg/kg, i.p.). The EDTA/Tris buffer and the slideswere examinedunder bright-fieldil- headof the cat waspositioned in a heavy-duty &ereo6xiEframe and lumination. For immunoperoxidase staining, a second set of slides was the calvarium wasexposed. Stainless steel screws were threadedinto rinsed four times for 20 min in TBS and incubated in biotinylated anti- the calvariumoverlying the frontal andparietal lobes in order to record rabbit IgG diluted I:2000 in TBS. After rinsing in TBS, they were the EEG. Another pair of screws were threaded into the orbital portion incubated for 1 hr in avidin-biotinylated horseradish peroxidase com- of the frontal bone to monitor electro-oculographic (EGG) activity. plex at a I: 100 dilution in TBS. The slides were then rinsed in TBS and Bipolar strut electrodes were implanted bilaterally into the lateral ge- peroxidase activity was visualized using equal parts 0.02% hydrogen niculate nuclei [A 5.5, L 9, H 5, according to Berman’s (1968) coor- peroxidase and 0. I % diaminobenzidine tetrahydrochloride (Sigma) in dinates]; these electrodes were used lo monitor ponto-geniculo-occipital TBS (pH 7.6) for 8-l 5 min. After a final three rinses (I 5 min each) in (PGO) waves. A Winchester plug, connected to these electrodes, and a TBS, the slides were rinsed in running water for 5 min followed by a chronic head-restraining device were bonded to the calvarium with distilled water rinse. They were counterstained in cresyl violet (Chroma), acrylic cement. A hole 4-5 mm in diameter was drilled in the calvarium dehydrated, and cleared in xylene. overlying the cerebellar cortex and covered with a bonewax plug. This Data analysis. In the present study, brainstem sections at the level of hole provided access to a cannula for drug microinjection.
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