Abstract
Bursting as well as tonic firing patterns have been described in various sensory systems. In the olfactory system, spontaneous bursts have been observed in neurons distributed across several synaptic levels, from the periphery, to the olfactory bulb (OB) and to the olfactory cortex. Several in vitro studies indicate that spontaneous firing patterns may be viewed as “fingerprints” of different types of neurons that exhibit distinct functions in the OB. It is still not known, however, if and how neuronal burstiness is correlated with the coding of natural olfactory stimuli. We thus conducted an in vivo study to probe this question in the OB equivalent structure of insects, the antennal lobe (AL) of the tobacco hornworm Manduca sexta. We found that in the moth's AL, both projection (output) neurons (PNs) and local interneurons (LNs) are spontaneously active, but PNs tend to produce spike bursts while LNs fire more regularly. In addition, we found that the burstiness of PNs is correlated with the strength of their responses to odor stimulation – the more bursting the stronger their responses to odors. Moreover, the burstiness of PNs was also positively correlated with the spontaneous firing rate of these neurons, and pharmacological reduction of bursting resulted in a decrease of the neurons' responsiveness. These results suggest that neuronal burstiness reflects a physiological state of these neurons that is directly linked to their response characteristics.
Highlights
Neurons in various sensory systems produce action potentials in brief bursts of high frequency discharge as well as in tonic patterns [1]
projection (output) neurons (PNs) and local interneurons (LNs) have distinct spontaneous spike patterns The spike traces of morphologically identified PNs, macroglomerular complex (MGC)-PNs and LNs were individually examined
When pooling all LNs the interspike intervals (ISIs) histogram displayed a skewed distribution, with the major peak occurring at an ISI similar to that from PNs and MGC-PNs and the tail including larger ISIs (Fig. 2E)
Summary
Neurons in various sensory systems produce action potentials in brief bursts of high frequency discharge as well as in tonic patterns [1]. At the OB level, one type of juxtaglomerular cells, the external tufted cells, intrinsically fire bursts of action potentials at theta frequency while other types of juxtaglomerular cells do not produce spike bursts spontaneously [3]. The intrinsic GABAergic interneurons at this layer rarely fire any action potential spontaneously [7]. These in vitro observations suggest that spontaneous firing patterns are different in different types of neurons within the OB circuit. Despite that bursting patterns are commonly observed, it is largely unexplored if neuronal burstiness could be correlated with the function of encoding natural olfactory stimuli in a predictable fashion
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