Organization of olfactory and multimodal afferent neurons supplying the calyx and pedunculus of the cockroach mushroom bodies

Nicholas J Strausfeld, Yongsheng Li

Research output: Contribution to journalArticle

98 Citations (Scopus)

Abstract

The mushroom bodies of neopteran insects are considered to be higher olfactory centers because their calyces receive abundant collaterals of projection neurons from the antennal lobes. However, intracellular recordings of mushroom body efferent neurons demonstrate that they respond to multimodal stimuli, implying that the mushroom bodies receive a variety of sensory cues. The present account describes new features of the organization of afferent neurons supplying the calyces of the cockroach Periplaneta americana. Afferent terminals segment the calyces into discrete zones, I, II, III, and IIIA, which receive afferents from 1) two discrete populations of sexually isomorphic olfactory glomeruli, 2) two types of male-specific olfactory glomeruli, 3) the optic lobes, and 4) multimodal interneurons that originate in protocerebral neuropils. In addition, intracellular recordings and dye fills show that at least four morphologically distinct GABAergic elements link many regions of the protocerebrum to the calyces. A new type of touch- sensitive centrifugal neuron has been identified terminating in the pedunculus. The dendrites of this afferent reside in satellite neuropil, beneath the mushroom body's medial lobe, which is supplied by collaterals from medial lobe efferent neurons and by terminals from the central complex. The role of this centrifugal cell in odorant sampling is considered. Golgi impregnation identifies other afferents in proximal regions of the calyx (zone IIIA) that also originate from satellite neuropils, suggesting major reafference from the medial lobes channeled through this region. The relevance of multimodal supply to the calyx in odorant discrimination is discussed as are comparisons between mushroom body organization in this phylogenetically basal neopteran and other taxa.

Original languageEnglish (US)
Pages (from-to)603-625
Number of pages23
JournalJournal of Comparative Neurology
Volume409
Issue number4
DOIs
StatePublished - Jul 12 1999

Fingerprint

Mushroom Bodies
Afferent Neurons
Cockroaches
Neuropil
Efferent Neurons
Olfactory Bulb
Periplaneta
Neurons
Touch
Interneurons
Dendrites
Cues
Insects
Coloring Agents
Population

Keywords

  • Afferent interneurons
  • GABA immunoreactivity
  • Insect brain evolution
  • Multimodal integration
  • Odor processing
  • Parallel processing

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

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abstract = "The mushroom bodies of neopteran insects are considered to be higher olfactory centers because their calyces receive abundant collaterals of projection neurons from the antennal lobes. However, intracellular recordings of mushroom body efferent neurons demonstrate that they respond to multimodal stimuli, implying that the mushroom bodies receive a variety of sensory cues. The present account describes new features of the organization of afferent neurons supplying the calyces of the cockroach Periplaneta americana. Afferent terminals segment the calyces into discrete zones, I, II, III, and IIIA, which receive afferents from 1) two discrete populations of sexually isomorphic olfactory glomeruli, 2) two types of male-specific olfactory glomeruli, 3) the optic lobes, and 4) multimodal interneurons that originate in protocerebral neuropils. In addition, intracellular recordings and dye fills show that at least four morphologically distinct GABAergic elements link many regions of the protocerebrum to the calyces. A new type of touch- sensitive centrifugal neuron has been identified terminating in the pedunculus. The dendrites of this afferent reside in satellite neuropil, beneath the mushroom body's medial lobe, which is supplied by collaterals from medial lobe efferent neurons and by terminals from the central complex. The role of this centrifugal cell in odorant sampling is considered. Golgi impregnation identifies other afferents in proximal regions of the calyx (zone IIIA) that also originate from satellite neuropils, suggesting major reafference from the medial lobes channeled through this region. The relevance of multimodal supply to the calyx in odorant discrimination is discussed as are comparisons between mushroom body organization in this phylogenetically basal neopteran and other taxa.",
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