Intracellular responses of olfactory bulb granule cells to stimulating the horizontal diagonal band nucleus

doi:10.1016/0306-4522(92)90496-O

Neuroscience

Volume 48, Issue 2, May 1992, Pages 363-369

https://doi.org/10.1016/0306-4522(92)90496-O Get rights and content

Abstract

The effects of centrifugal afferents on membrane potentials of identified granule cells in the main olfactory bulb were studied in anaesthetized rats. Cells were located in the granule cell layer using evoked field potential profiles, and trans-synaptic activation via antidromic stimulation of output cell axon collaterals. Intracellular recordings maintained for 4–30 min showed complex spontaneous spike dis-charges and allowed characterization of the cell's input resistance, and on some occasions its morphology following intracellular injection of Lucifer Yellow. Stimulation in the nucleus of the horizontal limb of the diagonal band, but not surrounding regions, produced hyperpolarizing responses in 13 of 27 cells in the granule cell layer; four of these were morphologically identified as granule cells of two types, in five the responses had reversal potentials more negative than the resting potential, and six were identified as granule cells by monosynaptic activation from output axon collaterals. A different set of three cells in the granule cell layer responded with depolarization.

The results are consistent with the inhibition of tonic activity of granule cells by the nucleus of the horizontal limb of the diagonal band, leading to disinhibition of mitral and tufted cells via dendrodendritic synapses of granule cells on mitral/tufted cell secondary dendrites.

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The contacted somata corresponded to granule cells by size and morphology, but morphological criteria alone are not enough to distinguish between granule cell and deep short-axon cell dendrites (Price and Powell, 1970b,c,e). Electrophysiological studies on the effect of the stimulation of HDB on the MOB have shown that the tonic inhibition on the mitral cells is reduced via inhibition of the granule cells (Nickell and Shipley, 1988; Kunze et al., 1991, 1992a,b). The application of acetylcholine in this area has diverse effects whereas the application of GABA on the granule cell layer is able to restrict the activity in this area (Duchamp-Viret et al., 1993).
In this work we have analyzed the targets of the GABAergic afferents to the main olfactory bulb originating in the basal forebrain of the rat. We combined anterograde tracing of 10 kD biotinylated dextran amine (BDA) injected in the region of the horizontal limb of the diagonal band of Broca that projects to the main olfactory bulb, with immunocytochemical detection of GABA under electron microscopy or vesicular GABA transporter (vGABAt) under confocal fluorescent microscopy. GABAergic afferents were identified as double labeled BDA-GABA boutons. Their targets were identified by their ultrastructure and GABA content. We found that GABAergic afferents from the basal forebrain were distributed all over the bulbar lamination, but were more abundant in the glomerular and inframitral layers (i.e. internal plexiform layer and granule cell layer). The fibers had thick varicosities with abundant mitochondria and large perforated synaptic specializations. They contacted exclusively GABAergic cells, corresponding to type 1 periglomerular cells in the glomerular layer, and to granule cells in inframitral layers. This innervation will synchronize the bulbar inhibition and consequently the response of the principal cells to the olfactory input. The effect of the activation of this pathway will produce a disinhibition of the bulbar principal cells. This facilitation might occur at two separate levels: first in the terminal tufts of mitral and tufted cells via inhibition of type 1 periglomerular cells; second at the level of the firing of the principal cells via inhibition of granule cells. The GABAergic projection from the basal forebrain ends selectively on interneurons, specifically on type 1 periglomerular cells and granule cells, and is likely to control the activity of the olfactory bulb via disinhibition of principal cells. Possible similarities of this pathway with the septo-hippocampal loop are discussed.
Physiology of the Main Olfactory Bulb
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The olfactory system consists of two parallel systems, the main olfactory system and the accessory olfactory system. This chapter focuses upon the neurophysiology of the main olfactory bulb (MOB), the first brain structure in the main olfactory system that processes olfactory signals relayed from olfactory receptor neurons (ORNs) in the nasal epithelium. The MOB has long been an attractive model to study cellular mechanisms underlying the encoding, transfer, processing, and decoding of sensory information. The field of olfaction has undergone explosive growth over the last decade. In large part, this growth has been driven by the discovery of odorant receptor genes, how receptor neurons expressing specific odorant receptors map onto the MOB, and the development of mammalian MOB slice preparations. This chapter focuses primarily on neurophysiological studies of the mammalian MOB from the last decade. Readers are referred to other sources that review earlier work on MOB neurophysiology (Mori, K., 1987; Nickell, W. T. and Shipley, M. T., 1992).
Olfactory bulb networks revealed by lateral olfactory tract stimulation in the in vitro isolated guinea-pig brain
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Intracellular recordings from mitral cells (Hamilton and Kauer, 1988) revealed that inhibition plays a central role in patterning these action potential trains. Presumably, most of the inhibitory potentials evoked in mitral cells by sensory stimulation arise from GABA released by local bulbar interneurons (Jahr and Nicoll, 1980; Isaacson and Strowbridge, 1998; Schoppa et al., 1998); extrinsic GABAergic fibers appear to innervate primarily neurons with processes in the GCL (Kunze et al., 1992). However, bulbar interneurons may be activated through multiple pathways, either locally within the bulb through dendrodendritic synapses made between granule cell dendrites and the lateral dendrites of mitral cells (Rall et al., 1966) or through “backward” connections made by axons of deep layer pyramidal cells in the piriform cortex (Nakashima et al., 1978; Neville and Haberly, 2003).
Olfactory information processing is mediated by synaptic connections between the olfactory bulbs (OBs) and piriform–limbic cortices. Limited accessibility using common in vivo and in vitro preparations has hindered previous attempts to define these synaptic interactions. We utilized the isolated guinea-pig brain preparation to overcome these experimental limitations. Previous studies demonstrated extensive functional preservation in this preparation maintained in vitro by arterial perfusion.
Field potential laminar profiles were performed with multi-channel probes in the OB following stimulation of both the lateral olfactory tract (LOT) and the anterior piriform cortex (APC). Current-source density analysis was carried out on laminar profiles to reconstruct current sinks/sources associated with intrinsic synaptic activities. LOT stimulation induced sequentially i) an antidromic population spike (at 2.66±0.39 ms) located in the mitral cell layer that was resistant to 100 Hz high-frequency stimulation (HFS) and 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) (10 μM), ii) a component located in the external plexiform layer at 3.85±0.63 ms that was unaffected by HFS, iii) a large amplitude potential (peak amplitude at 5.84±0.58 ms) generated in the external plexiform layer, abolished by HFS and CNQX, but not by bicuculline (50 μM), iv) a late response (onset at 20.00±2.94 ms) abolished by CNQX and enhanced by bicuculline. Stimulation of the APC also induced a late potential abolished by HFS and CNQX. Both APC-evoked and late LOT-evoked responses were abolished by a transverse cut to separate OB from APC.
These results demonstrate in an isolated mammalian brain preparation the presence of reciprocal synaptic interactions between the OB and piriform cortical structures.
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The olfactory bulb receives signals from olfactory sensory neurons and conveys them to higher centers. The mapping of the sensory inputs generates a reproducible spatial pattern in the glomerular layer of the olfactory bulb for each odorant. Then, this restricted activation is transformed into highly distributed patterns by lateral interactions between relay neurons and local interneurons. Thus, odor information processing requires the spatial patterning of both sensory inputs and synaptic interactions. In other words, odor representation is highly dynamic and temporally orchestrated. Here, we describe how the local inhibitory network shapes the global oscillations and the precise synchronization of relay neurons. We discuss how local inhibitory interneurons transpose the spatial dimension into temporal patterning. Remarkably, this transposition is not fixed but highly flexible to continuously optimize olfactory information processing.
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The interactions between excitatory mitral cells and inhibitory granule cells are critical for the regulation of olfactory bulb activity. Here we review anatomical and physiological data on the mitral cell–granule cell circuit and provide a quantitative estimate of how this connectivity varies as a function of distance between mitral cells. We also discuss the ways in which the functional connectivity can be altered rapidly during olfactory bulb activity.
Cholinergic modulation of sensory representations in the olfactory bulb
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We present a computational model of the mammalian olfactory bulb (OB) designed to investigate how cholinergic inputs modulate olfactory sensory representations. The model integrates experimental data derived from diverse physiological studies of cholinergic modulation of OB circuitry into a simulation of bulbar responses to realistic odorants. Experimentally-observed responses to a homologous series of odorants (unbranched aliphatic aldehydes) were simulated; realistic cholinergic inputs to the OB model served to increase the discriminability of the bulbar responses generated to very similar odorants. This simulation predicted, correctly, that missing cholinergic inputs to the OB would result in greater generalization between similar aliphatic aldehydes. Based on the assumption that the overlap between the neural representations of two sensory stimuli is predictive of their perceptual similarity, we tested this prediction in a behavioral experiments with rats. We show that, indeed, rats with selective lesions of cholinergic neurons that project to the OB and cortex discriminate less well between aliphatic aldehydes with similar carbon chain lengths than do rats that received sham lesions.

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Intracellular responses of olfactory bulb granule cells to stimulating the horizontal diagonal band nucleus

Abstract

Neurosci. Lett.

Neuroscience

Neuroscience

Prog. Neurobiol.

Brain Res.

Brain Res.

Brain Res.

Response of individual olfactory nerve cells to microelectrophoretically administered chemical substances

Pflu¨gers Arch.

Analysis of individual rabbit olfactory bulb neuron responses to the microelectrophoresis of acetylcholine, norepinephrine and serotonin synergists and antagonists

J. Pharmac. exp. Ther.

The afferent connections of the main and accessory olfactory bulb formations in the rat: an experimental HRP-study

J. comp. Neurol.

The olfactory system and Alzheimer's disease

Int. J. Neurosci.

Intracellular responses of olfactory bulb neurones to basal forebrain stimulation

The olfactory bulb

Cholinergic and catecholaminergic afferents to the olfactory bulb in the Hamster: a neuroanatomical, biochemical and histochemical investigation

J. comp. Neurol.