de Oliveira Pimentel, D.; (2009) Intratraglomerular communication in the mammalian olfactory bulb. Doctoral thesis , University of London.

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Abstract

The olfactory bulb (OB) is the first processing structure in the olfactory system it receives direct sensory input from the olfactory sensory neurons and relays processed information to the olfactory cortex and other structures in the brain. The axons from sensory neurons expressing the same olfactory receptor molecule converge onto the same discrete structure on the surface of the OB, termed glomerulus. Each glomerulus forms a modular unit which confines the single apical tufts of about 25 mitral cells (MC). Understanding how intraglomerular cells communicate with one another will therefore improve our understanding of how the glomerular network processes the olfactory signal. Using whole cell recordings from mitral cells in acute mouse olfactory bulb slices I have examined various modes of MC-MC communication. MC dendrites are known to release glutamate from their apical and lateral dendrites which has been shown to depolarize their own presynaptic dendrites (self excitation SE). I first examined the anatomical locus of SE by investigating its properties in intact versus dendrotomized (those with amputated tufts) MCs. While dendrotomized cells lacked detectable self excitatory potentials I have found that all morphologically identified MCs with an intact apical tuft displayed robust SE. This form of SE was mediated by Ca2+ permeable AMPA receptors as it was completely blocked by their specific antagonist Naphthyl-acethyl-spermine (NAS). Electrical coupling between MCs was assessed by injecting large hyperpolarizing pulses. I have found that MCs that shared the same glomerulus were always bidirectionally coupled via gap junctions though the magnitude of coupling (CC) was variable across different pairs. Action potentials evoked in one MC also results in EPSP-like depolarizations in intraglomerular partners (lateral excitation LE). In contrast to the previously mentioned forms of communication LE was not reliably present in all intraglomerular pairs. I have found LE is mainly a unidirectional form of communication, although both bidirectional and complete lack of measurable LE can also occur. The magnitude of LE varied independently of that of other forms of communication (CC and SE amplitude) as well as with morphometric characteristics of the apical tufts (number of nodes, surface area). Despite being dependent on glutamate receptors LE contrasted with SE in that it was insensitive to NAS and therefore is a distinct form of chemical communication that relies on different AMPA receptor subtypes. I have also investigated whether in vivo-relevant patterns of theta-burst stimulation (TBS) could evoke significant long-term changes in LE efficacy similar to those observed at axo-dendritic connections. This form of communication showed a unique sensitivity to TBS in that the polarity and amplitude of change in efficacy was linearly and inversely correlated with the initial strength of LE. Small connections were enhanced while larger ones depressed, the change in efficacy was accompanied with a change in paired pulse ratio consistent with a presynaptic change in release probability after TBS. All together these data show that SE, electrical coupling and LE are independent forms of intraglomerular communication which might serve independent roles on glomerular processing. While SE and electrical coupling have been shown to facilitate spike synchrony across the network, LE provides the OB with a means of modulating intraglomerular excitation in response to in vivo -relevant patterns of activity.

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