BioSystems 36 (1995) 101-108

Modeling insect olfactory neuron signaling by a network utilizing disinhibition
Evyatar Av-Ron*a9b, Jean-Pierre RosparsC
‘ B3E, INSERM IJ263, ISARS, Facultk de Mdecine Saint-Antoine. 27 rue Chaligny. 7S571 Paris Cedex 12. France bGroupe de Bioinformatique. URA 686, Ecole Normole SupCrieure, 46 rue d’ lllm, 75230, Paris Cedex 05, France =L.uboratoire de Biomktrie, lnstitut National de la Recherche Agronomique, 78026 Versailles Cedex, France

Received 24 February 1995; accepted 27 March 1995

Ah&met

A male moth locates a conspecific female by detecting her sexual-pheromone blend. This detection is carried out in the antenna1 lobe, the first stage of olfactory information processing, where local inhibitory neurons and projection (relay) neurons interact. Antennal-lobe neurons exhibit low-frequency (C 10 Hz) background activity and bursting (> 100 Hz) activity in response to pheromone stimulation. We describe this behavior by a realistic biophysical neuron model. The bursting behavior of the model is the result of both intrinsic cellular propertieS and network interaction. A slowly activating and inactivating calcium channel provides a depolarizing current for bursting and disinhibition is shown to be. a feasible network mechanism for triggering this calcium channel. Small neural networks utilizing disinhibition are presented with local neurons intercalated between receptor and projection neurons. The tiring behaviors of projection neurons in response to stimulation by the pheromone blend or its components are in accordance with experimental results. This network architecture offers an alternative view of olfactory processing from the classical architecture derived from vertebrate studies. Keywords: Insect olfaction; Ion conductance neuron model; Network disinhibition

1. Introduction

ed glomeruli,

The first stage of insect olfaction processing resides in the brain antenna1 lobes (ALs). Receptor neurons (RNs) of the antennae send afferent inputs into well-organized structures of the AL, call-

in which they make synapse with AL neurons. Two main types of AL neurons are found in glomeruli, local neurons (LNs) with arboriza-

?? Corresponding author, Tel.: +33 1 44738433;Fax: +33 I 43738462;E-mail: avron@b3e.jussieu.fr.

tions confined to the AL and projection neurons (PNs) with axons that relay information to higher brain centers in the protocerebrum (for reviews see Christensen and Hildebrand 1987a, Rospars 1988, Homberg et al. 1989, Masson and Mustaparta 1990, Boeckh et al. 1990, Hildebrand et al. 1992). As a case study we examined olfaction process-

0303-2647/95609.50 0 1995 Elsevier Science Ireland Ltd. All rights reserved
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1989). responds with excitation to Cl5 and blend. This small network (there are 86 000 RNs and 30 PNs in the MGC of M&UCU (Homberg et al. lc). Cl5 and blend or inhibitory response to all three. Our goal is to study neuronal signaling mechanisms in the MGC. Av-Ron. which are intercalated between RNs and PNs. We use a realistic biophysical model to describe the PNs of the network. b). 1992). Rospars/ BioSystems36 fT99.g. Intracellular recordings from PNs in the MGC show various types of responses to the two major components and sex-pheromone gland extract (see Fig. e.g. The sex pheromone blend is composed of a number of different compounds. The delay in PN excitation suggests that there are no direct synapses from RNs to PNs (Christensen et al. (a) Bal. 1989. two 16carbon compounds have been found ‘ major’ from quantitative and behavioral points of view. Boeckh et al. 1989). 50ng L Fig. This complex processes sex-pheromone inputs coded by specialized RNs. a blend of these two components is sufficient to induce upwind flight of males towards the odor source (Tumlinson et al. In wind tunnel experiments. The connections between neurons in the glomeruli in general and the MGC in particular can be summarized as follows. 2. In this article we examine disinhibition as a possible mechanism for neural processing and signal recognition. with its well defined biological function. Most (or all) LNs are GABAergic and probably inhibitory (Hoskins et al. i. We have chosen to describe four properties of this response: duration and spiking frequency of the burst. -c-15. 1990. . J. 1989). 1. Some neurons are found to be generalists. in the moth Munducu sex& (Kaissling et al. 1987b)). la. 625 ms. A second type of specialist exhibits excitation to one major component and inhibition to the other (e. Scale markers: 50 mV.e. a dienal (bombykal. For example. but exhibits no response to C15. 1989)). (b) Cl5 (c) Pheromone-gland wash. The RNs send excitatory input to LNs. Waldrop et al. the socalled macroglomerular complex (MGC) of male moths (which is also present in other insects. but not to Bal. Tumlinson et al. is attractive for a theoretical study. Masson and Mustaparta 1990. This blend was also found to elicit neuronal response similar to extract from the female sex-pheromone gland (see Fig. duration of the inactivation period and spiking frequency of the background activity. 9 in (Christensen et al. 1993).-P. Hildebrand et al. Early inhibition is indicated by open arrow. Bal) and a trienal mimicked by a 15carbon aldehyde (Cl 5).. 1989)). 1986. Sex pheromones released by female moths attract their conspecific males. see Figs.102 E. This system plays a crucial role for the survival and evolution of the species. twelve aldehydes have been identified. The response to blend is a mixture of the two (Fig. Other neurons are specialists. Neuron model PNs respond to an odorant stimulation with a burst followed by a period of inactivation (Fig. Taken with permission from Christensen and Hildebrand (1987b). Similar neuronal responses were found in other moth species (Christensen et al. or vice-versa. Bars indicate stimuli. 12 in (Christensen and Hildebrand. In this manner the biophysical features of the basic neural components can be related to the overall computational properties of the network. Of these. One type of specialist responds with excitation to Bal and blend. they exhibit either excitatory response to Bal. la). 1987). Response of a neuron to odor stimulation. cockroaches and honey bees (Rospars 1988.5) 101-108 ing in a specific glomerular AL neuropil.

W)tj2 = -45 mV acx) = 2.08. = -50 mV. 1991). Av-Ron 1994). K.= -72 mV. we assume the projection neuron (PN) has an oscillatory behavior (ca.. = 1 pFlcm2. V. = -35 mV a@+= 0.5. the values of the parameters that define the kinetics of the different currents were kept constant.-~J) and a leak current IL. i. &= I5 mWm2. Finally. = 2.3 mWm2.5 rnWcm2. The ordinary differential equations were solved numerically using the fourth-order Runge-Kutta method with a time step of 0. a@ = 0. = 5 @cm2 from t = 300 to 320 ms. Only two parameters were varied to achieve the different behaviors. Low-frequency activity and bursting behavior of neuron model. another local neuron (LNl) connected to LN2 is . low-frequency oscillations commence. 4a). &. 3a). a single neuron model was used.065.-P.2 (inflection point). For bursting behavior the currents Ia and ZKccalwere incorporated (Plant 1981. Av-Ron. Depicted are membrane potential V (solid line). &ca. Serial network A basic network utilizing disinhibition consists of four neurons in series (Fig. s = I. 1993). A typical behavior of the model is shown in Fig. see Ap per&x) consists of two inward currents (sodium INoand calcium ZcJ and three outward potassium currents (delayed ZK. P)rn = -31 mV atrn)0. This model was developed in a stepwise manner. intracellular calcium concentration C (dashed tine). 20 Hz.02. eventually bringing about the quiescence (inactive) period. 1977. a burst response is displayed. (see (7)).055. The steady-state functions are modeled as sigmoid curves. = 124 mV. Burst initiated by an input current Li. Av-Ron et al. KP= 0. For simplicity a single process is used for calcium diffusion.e. = I mS/cm2. = 0. intracellular calcium is removed (see curve C). As well the reversal potential for calcium is assumed to be constant.2 = -70 mV. Vc”). V.E.. V. This is mainly determined by the current IA. = 0.1. transient IA and calciumdependent ZK(. = 55 mV..006. J. and ZK are required (Hodgkin and Huxley 1952. For a single action potential the currents Z.5 m!Ycm2.Vi). r6 = IO ms.. For a short excitatory stimulation. the maximal conductance gig the activation and inactivation variables or functions. Rose and Hindmarsh 1989.0002. Results Fig. Wr. 3. a$) = -0. v(l)ro) = -20 mV. Rinzel and Lee 1987. 2. When connected to a local neuron (LN2) the low frequency spontaneous activity of LN2 is sufficient to inhibit the PN and keep it below the bursting threshold. Rospars/ BioSystems 36 (1995) 101-108 103 The biophysical model (Av-Ron 1994. During quiescence. For the PN to exhibit a bursting response to odor stimulation.01 ms. buffering and sequestration. the half maximum voltage Vi. & = 12. which has a slow time constant rb for inactivation (see curve Z?). Upon returning to resting levels. K = 0. and the slope a of the curve at this point. activating the current ZKlcol (see (10)) and inactivating the current I. and the driving force (V . Kd = 0. see right-hand side of Fig. Model parameters: C. FitzHugh 1961. In the absence of stimulation. 3.1. calcium channel activation X (solid line marked X) and transient potassium channel inactivation B (solid line marked B). the model exhibits slow oscillations (6 Hz with the specific values chosen for the parameters). calcium enters the cell. In this paper. gNU= 120 mS/cm2. the maximal potassium conductance g’ Aand the rate of calcium removal (R). During the burst. rx = 25 ms. With no stimulation. 2. Calcium was assumed to reside in a thin shell under the membrane. R = 0. The stimulation activates (variable x) the current Zca which remains active for the duration of the burst due to the slow time constant rX (see curve x). zr. An ion current Zi is described by the product of three MINIS. to exhibit both low 0 -60 1 0 ----__ _ _ ‘ _ 500 1000 Time (msec) 1500 2( and high firing frequencies the current IA was introduced (Connor et al. Av-Ron et al. V. determined by two parameters.

104 E. (b) Specialist network uti!ising disinhibition. a short excitatory response is elicited. 4a shows the behavior of a PN resulting from this serial network. required. 4b. la. This can be compared with observed experimental results where short odor stimulations (about 50 ms) triggered bursting responses (see Fig. When the inhibitory current is re-established the neuron returns to its spontaneous 3 Hz oscillations. Fig. However. 4a) when RNs a~ stimulated with odors A and/or B. For stimulation with a mixture of odorants A and B the PN responds as shown in Fig. At time 2.g. 4a. PN exhibits an excitatory response (see Fig. mimicking tonic inhibition by LN2) and exhibits slow spontaneous oscillations (3 Hz for the chosen parameters). C15) it is strongly inhibited by LN2 for the duration of the odorant stimulation and responds as shown in Fig. An initial inhibition is followed by a burst. 4c). For odors A and B. 4a) to stimulation with odor A. For stimulation with odorant A (e. the neuron receives inhibition (Z. (a) Generalist network utilising disinhibition. In the experimental recordings the duration of the burst coincides with the duration of stimulation (0. LNl inhibits LN2. Av-Ron. This simulation describes the experimentally observed behavior shown in Fig.2.5 @Ucm’ . allowing it to fire a burst. Both LNl and LN2 are excited simultaneously by their respective RNs. Neural networks of receptor (RN). 4a. a shorter period (120 ms) of disinhibition is sticient to obtain a bursting response. After a synaptic delay LN2 receives inhibition from LNl. for the model. The PN has the same properties as above. 3.2 s intracellular calcium concentration has reached its base level and the model begins to oscillate at 20 Hz. This input inhibits LN2 and consequently releases the .g. Bal) it behaves as shown in Fig. At time 0. Stimulation with both odors A and B elicits a ‘ mixed’response (see Fig. Rospars/BioSyslems 36 (1995) 101-108 a b c Fig. Responses to odor A or B is as (b). excluding the 20-Hz oscillation after time 2. local (LN) and projection (PN) neurons with excitatory (+) and inhibitory (-) connections. The duration of the burst depends on the intracellular calcium concentration which activates the current IKfcoJ and inactivates the current Zca The burst is followed by a period of inactivation during which intracellular calcium is removed.-P. 1 in Christensen and Hildebrand 1988). For stimulation with odorant B (e. (c) Specialist network based on the ‘ classical’ architecture of the vertebrate olfactory bulb with lateral inhibition. Therefore. PN exhibits an excitatory response (see Fig. When stimulated by the excitatory RNs. When the stimulation ceases the PN returns to its slow background activity (3 Hz).im = -0. 4a) to stimulation with odor B and an inhibitoryresponse (see Fig.5 s). LN2 inhibits the PN.5 s the inhibitory current is suppressed (mimicking inhibition of LN2 by LNl during odor stimulation) and the neuron exhibits its bursting response. During the first second 3. Parallel network A network based on inhibition and disinhibition is shown in Figure 3b. J.2 s shown in Fig. 4c. which leads to the disinhibition of the PN.

Rospars/ BioSystems 36 (1995) 101-108 105 PN which fires a burst of activity.. (Hayashi Hildebrand et al. due to different values of g” and R) and shows a burst in response to a short excitatory stimulation.. Behavior of projection-neuron model. = -5 fiA/cm* from r = 0.. Fig.1. 1. Disinhibition of neuron membrane potential Cell culture work suggests that the channel types used in the biophysical model are present in receptor (Zufall et al. firstly as a biophysical mechanism for explaining intracellular recordings (individual neuron properties) and secondly. intracellular calcium concentration (dashed line) and stimulating current (dotted line). Stengl 1994) and AL neurons and Hildebrand 1990.. (b) Constant inhibition IStim = -0.5 nNcm*) until r = 0. -.5 n 7 . . 4a on the right. Mercer et al. Depicted are membrane potential V (solid line).5 @cm* for the entire duration (0 to 2 s). Model parameters: as Fig.52 to 1 s. A decrease of the firing rate follows which brings about the lower intracellular calcium con- . .0025. except inhibition IS.____ .- / 0 500 1000 1500 2000 60- -60 r 0 . The mechanism of this response is as follows. Response to disinhibition (ISrim = 0 for t>0. (c) Constant inhibition Isrh = -0. This model exhibits intrinsic low-frequency background activity (6 Hz in Fig. R = 0.5 pA/cm* for the entire duration except inhibition I. called postinhibitory rebound (Selverston and Moulins 1985).0. as an information-processing mechanism (local network properties). .E.. Following the burst the PN is inactive and eventually returns to its low-frequency spontaneous background activity. Applying inhibition reduces the background activity further (Fig. = 0) the model exhibits 20-Hz background activity (I > 2.2 s).I. from 20 Hz on the right to 3 Hz on the left). 4. .50 to 0.500 1000 1500 2000 I” . Av-Ron.-P. J.5 to I s. Inhibition hyperpolarixes the membrane potential which in turn increases the threshold for tiring. 4. When inhibition is stopped (disinhibition) a bursting response occurs.h = -5 @/cm* from 0..5 s) includes a burst followed by a period of inactivation.5 s. 4a. 2 except fA = IO mS/crn*. a threshold for action potentials (activation of the sodium current) and a threshold for burst discharge (activation of the calcium current). 1992. Discussion In this paper we have studied disinhibition. This behavior results from the existence of two thresholds. . Without inhibition (I.i.. Klop penburg and Hildebrand 1995). 4.52 s and disinhibition (Istim = 0) from t = 0. ______-.. (a) Low frequency background activity resulting from constant inhibition (&. --. = -0. 1995. 2 and 20 Hz in Fig. 1991.

B]lq.. The depolarization of the LN brought about the inactivation of the PN. However.WJ/r.( I’ ) . Conversely.. Presented here is a simple biophysical model which can describe the qualitative behavior observed in PNs. D&inhibition in local-circuit processing The local circuit network is derived from experimental evidence. This mechanism is similar to that of Fig. Rospars/BioSysrems36 (1995) 101-108 centration C. Av-Ron. where the inactivation component is the current IKIca. I&inhibition of thalamocortical neurons reduces the inactivation of the low-threshold calcium current bringing about a rebound calcium plateau which causes a burst of action potentials (Jahnsen and Llinas 1984. hyperpolarizing the LN caused an increase in activity of the PN.2.-P. Shepherd and Greer 1990). Acknowledgements E. Rospars et al. Kloppenburg and Hildebrand 1995). France. These arrangements are in addition to the direct connec- tions from RN terminals onto LN and PN dendrites. If C would also increase rapidly the system would reach a stable oscillation as seen on the right-hand side of Fig. 1992). dXldt = [X.g.-IIC. 3c) of the vertebrate olfactory bulb in term of information processing. . This may be examined in relation to both neuronal development (Lockery and Spitzer 1992) and neuromodulation (Mercer et al. disinhibition provides an altemative to lateral inhibition’ as a functional role for inhibitory LNs in a network. More generally. (d) Correlation between activities in LN and PN pairs was found both in the MGC and regular glomeruli. 4a.g. When inhibition is removed the membrane depolarizes rapidly. 4a.XJ/r. (c) Most (or all) of the LNs are probably inhibitory intemeurons (Hildebrand et al. However. AppediX C. disinhibition may also apply to the vertebrate olfactory bulb because serial synapses between dendrites of presumed inhibitory LNs within the glomeruli have been documented (Pinching and Powell 1971. e. White 1972). the differences in terms of information processing between the ‘ classical model’ (e.R. 1993). et al. it is not evident whether the disinhibition model is capable of coding the quantitative features of the olfactory message. C (1) (2) (3) (4) (5) . dBldt = [B. 1995. the sensitivity of the model to parameter changes should be studied. (b) In some PNs (Fig. One possible advantage of disinhibition over excitation is that the PNs spontaneously return to the resting (inactive) state. instigating a positive feedback which results in the burst discharge. However this is not the case. Av-Ron was supported by program ‘ Poste Vert’ . INSERM. In conclusion. 1994) and the model of disinhibition remain to be further investigated.( J’ ) .-ZIK-IA-IK(Col-IL dWldt = [ W. The next step would be to choose parameters based on patch clamp experiments. 4. The disinhibition model proposed offers an alternative to the ‘ classical’ model (Fig. The mechanisms of disinhibition observed in the insect glomerulus and in the vertebrate reticular thalamic nucleus seem analogous.-IN.. whereas excitatory mechanisms may lead to propagating waves of activity (Wilson and Bower 1989). the slow increase in C results in a relatively weak current IK(c+ This allows the firing frequency and consequently the depolarizing calcium current to increase.( V). lc) the burst response is preceded by a short hyperpolarization (Christensen and Hildebrand 1988). 1993).. 1993). and the reciprocal contacts between these dendrites (cf. concentrations of A and B for specialist PNs (parallel network). This shows that at least some PN excitation is the result of disinhibition (Christensen et al. ratio of concentrations A:B for generalist PNs (serial network). Steriade. (a) The latency in response of PNs in comparison with LNs suggests that PNs do not receive direct excitatory inputs from receptor cells (Christensen and Hildebrand 1987.dVldt=I.106 E.J. L&rsky and Rospars 1993. Rospars and Fort 1994. Christensen et al. As well.(V) dCldt = K&-I& .

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