© 2001 by The Society for Integrative and Comparative Biology
Gaseous Oxides and Olfactory Computation1
1 Biological Computation Research Department Bell Laboratories, Lucent Technologies, 600 Mountain Avenue, Murray Hill, New Jersey 07974
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The gaseous neurotransmitters nitric oxide (NO) and carbon monoxide (CO) are prominent and universal components of the array of neurotransmitters found in olfactory information processing systems. These highly mobile communication compounds have effects on both second messenger signaling and directly on ion channel gating in olfactory receptors and central synaptic processing of receptor input. Olfactory systems are notable for the plasticity of their synaptic connections, revealed both in higher-order associative learning mechanisms using odor cues and developmental plasticity operating to maintain function during addition of new olfactory receptors and new central olfactory interneurons. We use the macrosmatic terrestrial mollusk Limax maximus to investigate the role of NO and CO in the dynamics of central odor processing and odor learning. The major central site of odor processing in the Limax CNS is the procerebral (PC) lobe of the cerebral ganglion, which displays oscillatory dynamics of its local field potential and periodic activity waves modulated by odor input. The bursting neurons in the PC lobe are dependent on local NO synthesis for maintenance of bursting activity and wave propagation. New data show that these bursting PC interneurons are also stimulated by carbon monoxide. The synthesizing enzyme for carbon monoxide, heme oxygenase 2, is present in the neuropil of the PC lobe. Since the PC lobe exhibits two forms of synaptic plasticity related to both associative odor learning and continual connection of new receptors and interneurons, the use of multiple gaseous neurotransmitters may be required to enable these multiple forms of synaptic plasticity.
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INTRODUCTION |
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Olfactory systems are remarkable both for the sensitivity and scope of their molecular detection ability and for the plasticity of their synaptic programming. At the limits of odor sensitivity only a few dozen molecules are sufficient for detection and categorization of the odor sampled by the receptor surface. Synaptic plasticity in olfaction is evident both in the way odor cues participate in higher-order associative learning (Sahley, 1990
; Eichenbaum, 1998) and in the maintenance of olfactory function during continual postembryonic neurogenesis at the sensory periphery (Chase and Rieling, 1986; Sandeman and Sandeman, 1996; Weiler and Farbman, 1997; Weiler et al., 1999) and in central odor processing sites (Harzsch et al., 1999; Sandeman et al., 1998; Zakharov et al., 1998; Kirschenbaum et al., 1999; Murray and Calof, 1999; Mellon and Tewari, 2000).
Gaseous neurotransmitters such as nitric oxide (NO) and carbon monoxide (CO) are prominent and universal constituents of the array of neurotransmitters found in olfactory systems, both centrally and at the receptor surface (Breer and Shepherd, 1993; Muller and Hildebrandt, 1995; Hildebrand and Shepherd, 1997; Zufall and Leinders-Zufall, 1997; Gelperin, 1999; Koh and Jacklet, 1999; Moroz, 2001). There is evidence that NO and CO play a role in olfactory synaptic plasticity (Robertson et al., 1994, 1995; Müller, 1996; Okere et al., 1996; Teyke, 1996; Kendrick et al., 1997) as well as developmental guidance and plasticity in a variety of systems (Nighorn et al., 1998; Cramer and Sur, 1999; Renteria and Constantine-Paton, 1999; Schachtner et al., 1999; Van Wagenen and Rehder, 1999; Wildemann and Bicker, 1999). More generally, gaseous neurotransmitters, particularly NO, are prime candidates for a feedback signal from postsynaptic to presynaptic compartments mediating synaptic plasticity and Hebbian learning in mammals (Altememi and Alkadhi, 1999; Haul et al., 1999; Ko and Kelly, 1999; Lu et al., 1999; Moody et al., 1999; Murphy and Bliss, 1999; Wilson et al., 1999; Zhuo et al., 1999) and mollusks (Bravarenko et al., 1995; Teyke, 1996; Fossier et al., 1999; Malyshev and Balaban, 1999)
We are investigating the role of small mobile neurotransmitters such as NO and CO in the olfactory system of the terrestrial mollusk Limax maximus, a macrosmatic species with highly developed odor learning ability (Sahley, 1990; Sekiguchi et al., 1997; Kimura et al., 1998b; Gelperin, 1999), also well described in Helix (Balaban et al., 1994; Teyke, 1995) The olfactory systems of Limax and Helix display a number of general design features found in mammalian olfaction, including continual receptor turnover (Chase and Rieling, 1986) and postembryonic neurogenesis in central olfactory processing sites (Zakharov et al., 1998). The major central site of odor processing is the procerebral (PC) lobe of the cerebral ganglion, which receives direct input from receptors (Zaitseva, 1991; Chase and Tolloczko, 1993). The PC lobe has oscillatory dynamics evident in the periodicity of its local field potential (Gelperin and Tank, 1990; Kleinfeld et al., 1994; Kawahara et al., 1997; Kimura et al., 1998a) and supports activity wave propagation from its apex to base at approximately 1 Hz (Ermentrout et al., 1998; Inoue et al., 1998; Kimura et al., 1998a; Nikitin and Balaban, 1999). The oscillatory nature of LFP recordings in the PC lobe arises from the periodicity of wave propagation past the recording site. If LFP recordings are made simultaneously from apex and base, a phase delay is measured during wave propagation in both Limax (Ermentrout et al., 1998) and Helix (Fig. 1). The oscillatory LFP activity recorded with saline-filled glass electrodes in vitro is also characteristic of some periods of LFP recordings made with implanted fine-wire electrodes in vivo (Cooke and Gelperin, 2001).
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NO and CO production in the PC lobe
Because the anatomy of the olfactory information processing pathways in Limax and Helix strongly suggests that the PC lobe is the major central site of olfactory processing, we wished to assess the presence of synthesizing enzymes for NO and CO in the PC lobe. The NADPH diaphorase reaction for nitric oxide synthase (NOS) gives a very prominent reaction product in the neuropil regions of the PC lobe and in some cells and fiber tracts within the cell layer (Fig. 2A) (Cooke et al., 1994
; Sánchez-Alvarez et al., 1994; Gelperin et al., 2000). The PC lobe has two distinct neuropil regions, the internal mass (IM) at the base of the lobe where neurites of intrinsic PC interneurons interact, and the terminal mass (TM) adjacent to the cell layer, where processes of the olfactory afferent fibers interact with neurites of intrinsic PC interneurons (Kawahara et al., 1997; Ratté and Chase, 1997). The tentacular ganglion immediately adjacent to the olfactory receptor surface also reacts strongly for NADPH diaphorase activity (Fig. 2B). Approximately 15% of the olfactory receptors synapse in the tentacular ganglion (Chase and Tolloczko, 1993) hence some of the input to the PC lobe may be second order.
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CO is synthesized in neural tissue by heme oxygenase 2 (HO2), which reacts with heme to generate CO, iron, and biliverdin, which is immediately reduced to bilirubin (Maines, 1993
; Dore et al., 1999). Using a polyclonal antibody to rat native HO2 (StressGen Biotechnologies, Victoria, CA), we consistently found (six preparations) a discrete region of punctate staining at the base of the IM neuropil in the Limax PC lobe (Fig. 3A) and in the PC lobe of Helix (Fig. 3B). The cells of origin for the fiber staining shown in Figure 3 are at present unknown. There are, however, numerous HO2 immunoreactive somata outside the PC lobe, particularly in the subesophageal ganglia (Figs. 4A, B, 5). Since we know that pedal and buccal cells have neurites in the PC lobe (Chase and Tolloczko, 1989; Gelperin and Flores, 1997; Ratté and Chase, 1997), it is quite plausible that the somata belonging to the HO2 immunoreactive fibers at the base of the IM neuropil are in the subesophageal ganglia. As with NOS staining, the tentacular (=digitate) ganglion also shows clear staining for HO2 in both Helix (Fig. 6) and Limax (data not shown). We have not examined the buccal ganglia for HO2 staining. The wide distribution of HO2 immunoreactive cells and fibers in the Helix CNS strongly suggests that CO may play a substantial role in neuronal communication in a variety of CNS circuits in Helix and in other terrestrial gastropods.
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NO production is necessary for LFP oscillation in the PC lobe
We have shown previously that inhibition of NOS slows and can stop the cellular activity responsible for the LFP oscillation in the PC lobe (Gelperin, 1994a
; Gelperin et al., 2000). Application of either oxyheme proteins as extracellular NO scavengers or inhibitors of NOS such as substituted arginines can reversibly halt the LFP oscillation. Intracellular recordings from the bursting PC neurons responsible for the LFP oscillation and wave propagation (Kleinfeld et al., 1994) show that they are stimulated by NO application and become quiescent upon inhibition of NO synthesis (Gelperin et al., 2000). The caged NO compound nitrosylpentachlororuthenate (NPR) (Murphy and Bliss, 1999) provides a particularly convenient and effective means of NO application. Using PC lobe preparations bathed in NPR and very localized uncaging flashes, we found that small regions (30–50 µm diameter) of the PC lobe can be stimulated to produce high frequency activity independent of the ongoing macroscopic LFP oscillation and wave propagation (Fig. 7). Flashes delivered in the absence of NPR are without effect. This is consistent with the possibility that localized afferent input arising from odor stimulation could stimulate local activity in the PC lobe not evident in the macroscopic measurement of the oscillating LFP (Teyke and Gelperin, 1999).
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CO application alters LFP oscillation frequency
A new reagent for temporally and spatially controlled application of CO to neural tissue has recently been synthesized (Kao and Keitz, 1997
). This molecule, NV/CO, is shown in Figure 8A, while the photolytic reaction triggered by near UV stimulation is shown in Figure 8B. Calibration of NV/CO using rat aortic smooth muscle cells and measuring cGMP content shows the activity of NV/CO to parallel that obtained with CO-containing solutions (Kao and Keitz, 1997). We have found that CO application to Limax PC lobes using flash photolysis of NV/CO increases the frequency of the ongoing LFP oscillation (Fig. 9) in a dose-dependent manner (Fig. 10). Since the caged CO compound also liberates benzene upon photolysis, control experiments were done applying benzene at 10, 20 and 50 µM to the PC lobe with either no effect or a slight reduction in LFP oscillation frequency (data not shown). These concentrations span a range more than 10 fold higher that the calculated peak concentration of benzene resulting from uncaging of NV-CO.
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DISCUSSION |
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The PC lobe of Limax appears to use two gaseous neurotransmitters, NO and CO, in maintaining its normal oscillatory dynamics and wave propagating mode (Gelperin, 1994b, 1999
; Gelperin et al., 1996). Two lines of evidence suggest that maintenance of oscillatory dynamics and wave propagation in the Limax PC lobe is necessary for odor learning and odor discrimination. On the assumption that structure and dynamics of the Helix PC lobe are very similar to those of Limax (cf., Fig. 1 and [Ratté and Chase, 2000]), the finding that injecting an inhibitor of NOS into Helix blocks odor learning (Teyke, 1996) could be interpreted to mean that blocking the oscillation and wave propagation of the Helix PC lobe blocks odor learning. The Helix PC lobe stains densely for NOS (Cooke et al., 1994) and, as in Limax, has odor-modulated wave propagation from apex to base (Nikitin and Balaban, 2000). A critical test of this interpretation is to measure the effect of the injected NOS inhibitor on PC lobe activity using implanted electrodes in the intact animal, which has recently been demonstrated (Cooke and Gelperin, 2001). Another type of evidence linking PC oscillations and wave propagation to odor memory access was obtained from odor-elicited responses in the peritentacular nerve (PTN) of Limax studied in nose-brain preparations prepared from pretrained slugs (Teyke and Gelperin, 1999). The PTN discharge is specific to odors which have been appetitively conditioned (Peschel et al., 1996). Reversibly blocking the oscillations in the PC lobe did not impair recognition of a conditioned odor but did reduce the differential PTN response to closely related odors (Teyke and Gelperin, 1999). This suggests that blocking the PC lobe oscillation in vivo would degrade odor discrimination between similar odors, which has been observed in honeybee after blocking odor-elicited oscillations in the antennal lobe and mushroom body by the in vivo application of picrotoxin (Stopfer et al., 1997).
Odor-elicited oscillations are a general feature of olfactory systems (Adrian, 1942; Hughes and Mazurowski, 1962; Hughes et al., 1969; Laurent and Naraghi, 1994; Delaney and Hall, 1996; Dorries and Kauer, 2000) and there is great interest in deciphering their computational role (Gray, 1994; Gelperin, 1999; Hopfield, 1999; Lam et al., 2000). The odor-elicited oscillations in mammalian olfactory bulb may be mediated or augmented by NO, as the olfactory bulb stains densely for NOS (Bredt et al., 1991; Vincent and Kimura, 1992; El-Husseini et al., 1999; Nakamura et al., 1999) and NO affects the excitability of mammalian central neurons (Pape and Mager, 1992; Pineda et al., 1996; Yang and Hatton, 1999). NO acts within a volume centered on its site of synthesis with radius of action dependent on the geometry of its source as well as the types and abundance of molecules which bind or inactivate NO (Philippides et al., 2000).
Nitric oxide is known to affect growth and migration of neurons and glial cells (Cramer and Sur, 1999; Renteria and Constantine-Paton, 1999; Van Wagenen and Rehder, 1999; Chen et al., 2000). Since the postembryonic PC lobe continually receives new input fibers from newly generated receptors (Chase and Rieling, 1986) and generates new neurons for at least several months after hatching (Zakharov et al., 1998), NO may play a role in the plasticity required to integrate these new synapses into the existing PC lobe circuitry.
Carbon monoxide, like NO, is a small highly mobile neurotransmitter with a clear association with the olfactory system. Olfactory receptor neurons and elements of the olfactory bulb in mammals have the highest concentration of HO2 in the entire mammalian CNS (Ewing et al., 1993; Verma et al., 1993). Studies on olfactory receptors provide particularly clear evidence for a role for CO in responses to odor ligands (Ingi and Ronnett, 1995; Ingi et al., 1996a, b; Zufall and Leinders-Zufall, 1997). The role of CO in central olfactory circuits is as yet unknown. CO in the Limax PC lobe may be involved in setting the burster neuron oscillation frequency and hence the frequency of the LFP oscillation or in mechanisms of synaptic plasticity for odor learning or connectional plasticity due to new synapse formation during adult neurogenesis. Experiments to probe the role of endogenous CO production in the PC lobe are complicated by the need to selectively inhibit HO2 without inhibiting NOS or soluble guanylyl cyclase (Meffert et al., 1994). In some systems selective inhibition of HO2 can be accomplished by applying appropriate concentrations of chromium mesoporphyrin IX (Appleton et al., 1999). In cultures of cerebellar granule cells, CO modulates the NO-cGMP signaling system (Ingi et al., 1996a). The interactions between NO and CO generating systems have been reviewed recently (Maines, 1997).
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ACKNOWLEDGMENTS |
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We thank J. W. Wang and J. Flores for collecting some of the data used in this paper.
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FOOTNOTES |
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1 From the Symposium on Nitric Oxide in the Invertebrates: Comparative Physiology and Diverse Functions presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 4–8 January 2000, at Atlanta, Georgia.
2 E-mail: CNSAG{at}Bell-Labs.com
3 Present address of J. P. Y. Kao is Medical Biotechnology Center, University of Maryland School of Medicine, Baltimore, Maryland 21201
4 Present address of I. R. C. Cooke is Macfarlane Burnet Centre for Medical Research, Fairfield, Victoria, Australia 3078
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