Molecular Features of Odorants Systematically Influence Slow Temporal Responses Across Clusters of Coordinated Antennal Lobe Units in the MothManduca sexta

Abstract

Behavioral studies of olfactory discrimination and stimulus generalization in many species indicate that the molecular features of monomolecular odorants are important for odor discrimination. Here we evaluate how features, such as carbon chain length and functional group, are represented in the first level of synaptic processing. We recorded antennal lobe ensemble responses in the moth Manduca sexta to repeated 100-ms pulses of monomolecular alcohols and ketones. Most units exhibited a significant change in spike rate in response to most odorants that outlasted the duration of the stimulus. Peristimulus data were then sampled over 780 ms for each pulse of all odorants. Factor analysis was used to assess whether there were groups of units with common response patterns. We found that factors identified and represented activity for clusters of units with common temporal response characteristics. These temporally patterned responses typically spanned 780 ms and were often dependent on carbon chain length and functional group. Furthermore, cross-correlation analysis frequently indicated significant coincident spiking even during spontaneous activity. However, this synchrony occurred mainly between units recorded on the same tetrode. In a final analysis, the Euclidean distance between odor responses was calculated for each pair of odorants using factors as dimensions. The distance between responses for any two odorants was maximized by approximately 240 ms. This time course corresponded to the brief sequence of coordinated bursts across the recorded population. The distance during this period was also a function of systematic differences in molecular features. Results of this Euclidian analysis thus directly correlate to previous behavioral studies of stimulus generalization in M. sexta.

Circadian regulation of insect olfactory learning

“…Early studies (15,19) indicated that the MBs play a critical role in olfactory memory and suggested that olfactory memories are formed upstream of the output neurons of the MBs, which determine performance, and that the memory trace probably lies within the MBs. More recently, studies using food or electric shock as a US in a variety of insects, including bees (38), flies (39), and moths (20), have shown that learning-dependent changes in neural activity also occur as early as the antennal lobe, which therefore appears to be the first site in the olfactory pathway for convergence of the conditioned stimuli and US and thus may be a site for the circadian regulation of memory acquisition in the cockroach. US pathways that lead to this convergence are not well understood; however, there are data that suggest that aminergic input may play a pivotal role.…”

“…Olfactory learning in insects, in particular, is widespread and has been extensively used as a model for studies on the behavior, neurobiology, genetics, and molecular biology of learning and memory in bees (e.g., 16,17), fruit flies (15,18,19), and moths (20). As a consequence, much is understood about the anatomical substrate and physiological and molecular mechanisms of insect olfactory learning.…”

Learning about natural variation of odor mixtures enhances categorization in early olfactory processing

“…We have shown that plasticity in the AL acts to increase separation of patterns evoked by odors that have been differentially associated with food (Fernandez et al, 2009). However, research on olfactory coding and plasticity has focused on pure odors or simpler mixtures (Daly et al, 2004;Fernandez et al, 2009;Stopfer et al, 2003;Deisig et al, 2006Deisig et al, , 2010Guerrieri et al, 2005;Linster and Smith, 1999) rather than on the more complex odor problems presented by flowers. Even when more complex odor mixtures were used, odor compositions were not systematically varied as odors would vary from flower to flower of the same species in natural scenes.…”

Extracellular Wire Tetrode Recording in Brain of Freely Walking Insects

“…Correlate specific electrical impulses to the activity of single neurons. Follow spike sorting procedures laid out in detail elsewhere 10,14,18 . Use the program KlustaKwik (version 1.5, author K. Harris, Rutgers University) to generate initial, automated clustering.…”