Electrophysiological Evidence for a Chemotopy of Biologically Relevant Odors in the Olfactory Bulb of the Channel Catfish

Nikonov, Alexander A.; Caprio, John

doi:10.1152/jn.2001.86.4.1869

Cited by 85 publications

(74 citation statements)

References 73 publications

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“…These two independent methods therefore confirm for Manduca that different classes of odorants are represented as overlapping but distinct spatial patterns of activity in the AL glomeruli. Accumulating evidence from the vertebrate OB (Rubin and Katz, 1999;Fuss and Korsching, 2001;Nikonov and Caprio, 2001) and insect AL (Gao et al, 2000;Vosshall et al, 2000;Galizia and Menzel, 2001) also supports this combinatorial spatial model.…”

Section: Discussionmentioning

confidence: 75%

Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

2004

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In the insect antennal lobe, odor discrimination depends on the ability of the brain to read neural activity patterns across arrays of uniquely identifiable olfactory glomeruli. Less is understood about the complex temporal dynamics and interglomerular interactions that underlie these spatial patterns. Using neural-ensemble recording, we show that the evoked firing patterns within and between groups of glomeruli are odor dependent and organized in both space and time. Simultaneous recordings from up to 15 units per ensemble were obtained from four zones of glomerular neuropil in response to four classes of odorants: pheromones, monoterpenoids, aromatics, and aliphatics. Each odor class evoked a different pattern of excitation and inhibition across recording zones. The excitatory response field for each class was spatially defined, but inhibitory activity was spread across the antennal lobe, reflecting a center-surround organization. Some chemically related odorants were not easily distinguished by their spatial patterns, but each odorant evoked transient synchronous firing across a uniquely different subset of ensemble units. Examination of 535 cell pairs revealed a strong relationship between their recording positions, temporal correlations, and similarity of odor response profiles. These findings provide the first definitive support for a nested architecture in the insect olfactory system that uses both spatial and temporal coordination of firing to encode chemosensory signals. The spatial extent of the representation is defined by a stereotyped focus of glomerular activity for each odorant class, whereas the transient temporal correlations embedded within the ensemble provide a second coding dimension that can facilitate discrimination between chemically similar volatiles.

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Section: Discussionmentioning

confidence: 75%

Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

2004

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“…Studies using calcium imaging (Friedrich and Korsching, 1997;Friedrich and Korsching, 1998) and physiological recording (Nikonov and Caprio, 2001), to characterize the activity patterns elicited in the olfactory bulb by amino acids and bile salts, have demonstrated that the medial regions of the bulb process bile salt input and the lateral regions amino acids and nucleotides. This chemotopy, which appears to separate the processing of feeding cues (amino acids) from social cues (bile salts), is present in both channel catfish (Nikonov and Caprio, 2001;Nikonov et al, 2005) and zebrafish (Friedrich and Korsching, 1998). Thus the loss of behavioral responses to the amino acids but not taurocholic acid in the lre mutant suggests that the defect may result in part from the disruption and or loss of the sensory fibers in the lateral chain of glomerular modules that respond to amino acids.…”

Section: Segregation Of Physiological Responses Accompanies Distinct mentioning

confidence: 99%

Isolation and characterization of the laure olfactory behavioral mutant in the zebrafish, Danio rerio

Vitebsky

Reyes

Sanderson

et al. 2005

Developmental Dynamics

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To initiate a genetic analysis of olfactory development and function in the zebrafish, Danio rerio, we developed a behavioral genetic screen for mutations affecting the olfactory sensory system. First, we characterized olfactory responses of wild-type zebrafish to various odors. We found that 3-day-old juvenile zebrafish reacted to the amino acid L-cysteine with an aversive behavioral response. We isolated one mutant, laure (lre), which showed no aversive behavioral response to L-cysteine at 3 days of development, and carried out a preliminary characterization of this mutant's defects. We found that lre mutant fish were also defective in their response to L-serine and L-alanine, but not to taurocholic acid, as young adults. In addition, lre mutant fish had significantly fewer primary olfactory sensory neurons than normal, and the axons of these neurons did not form the characteristic axon termination pattern in the developing olfactory bulb. Nevertheless, the olfactory epithelium of lre mutant fish showed normal or near normal electrophysiological responses to several odorants. Our data suggest that the behavioral defects observed in the lre mutant result from the disruption of the developing olfactory sensory neurons and their axonal connections within the olfactory bulb. The isolation of the lre mutant shows that our behavior-based screen represents a viable approach for carrying out a genetic dissection of olfactory behaviors in this vertebrate model system. Developmental Dynamics 234:229 -242, 2005.

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“…In this ex vivo preparation, the lateral region of the lamprey olfactory bulb was a locus for amino acid responses and the dorsal region of the sea lamprey olfactory bulb responded to the steroid bile acid taurocholic acid in all cases, to both taurocholic acid and the steroid pheromones in 30% of cases, and to amino acids, taurocholic acid and pheromones in 50% of cases, and was the only region with cases that responded to taurocholic only (20%). Amino acids activate the lateral olfactory bulb region in teleost fish (Hansen et al, 2003;Hara and Zhang, 1998;Fujita et al, 1991;Hara, 2001, 2004;Friedrich and Korsching, 1998;Nikonov and Caprio, 2001) and in the larval stage of the amphibian Xenopus laevis (Gliem et al, 2013). However, while the olfactory system in teleosts responds to a wide variety of basic, acidic and aromatic amino acids (Hansen et al, 2003;Laberge and Hara, 2001), the lamprey olfactory system responds only to basic amino acids (Li et al, 1995).…”

Section: Discussionmentioning

confidence: 99%

“…However, while the olfactory system in teleosts responds to a wide variety of basic, acidic and aromatic amino acids (Hansen et al, 2003;Laberge and Hara, 2001), the lamprey olfactory system responds only to basic amino acids (Li et al, 1995). In teleosts, primarily bile acids and sex pheromones activate glomeruli in the medial region (Hansen et al, 2003;Hara et al, 1998;Fujita et al, 1991;Hara, 2001, 2004;Friedrich and Korsching, 1998;Nikonov and Caprio, 2001). In Xenopus, sulphated steroids stimulate the dorsal and medial region of the main olfactory system, rather than the lateral region (Sansone et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Odorant organization in the olfactory bulb of the sea lamprey

Green

Boyes

McFadden

et al. 2017

Journal of Experimental Biology

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Olfactory sensory neurons innervate the olfactory bulb, where responses to different odorants generate a chemotopic map of increased neural activity within different bulbar regions. In this study, insight into the basal pattern of neural organization of the vertebrate olfactory bulb was gained by investigating the lamprey. Retrograde labelling established that lateral and dorsal bulbar territories receive the axons of sensory neurons broadly distributed in the main olfactory epithelium and that the medial region receives sensory neuron input only from neurons projecting from the accessory olfactory organ. The response duration for local field potential recordings was similar in the lateral and dorsal regions, and both were longer than medial responses. All three regions responded to amino acid odorants. The dorsal and medial regions, but not the lateral region, responded to steroids. These findings show evidence for olfactory streams in the sea lamprey olfactory bulb: the lateral region responds to amino acids from sensory input in the main olfactory epithelium, the dorsal region responds to steroids (taurocholic acid and pheromones) and to amino acids from sensory input in the main olfactory epithelium, and the medial bulbar region responds to amino acids and steroids stimulating the accessory olfactory organ. These findings indicate that olfactory subsystems are present at the base of vertebrate evolution and that regionality in the lamprey olfactory bulb has some aspects previously seen in other vertebrate species.

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Electrophysiological Evidence for a Chemotopy of Biologically Relevant Odors in the Olfactory Bulb of the Channel Catfish

Cited by 85 publications

References 73 publications

Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe

Isolation and characterization of the laure olfactory behavioral mutant in the zebrafish, Danio rerio

Odorant organization in the olfactory bulb of the sea lamprey

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