Showing papers by "Nicholas J. Strausfeld published in 1998"

Evolution, Discovery, and Interpretations of Arthropod Mushroom Bodies

Abstract: Mushroom bodies are prominent neuropils found in annelids and in all arthropod groups except crustaceans. First explicitly identified in 1850, the mushroom bodies differ in size and complexity between taxa, as well as between different castes of a single species of social insect. These differences led some early biologists to suggest that the mushroom bodies endow an arthropod with intelligence or the ability to execute voluntary actions, as opposed to innate behaviors. Recent physiological studies and mutant analyses have led to divergent interpretations. One interpretation is that the mushroom bodies conditionally relay to higher protocerebral centers information about sensory stimuli and the context in which they occur. Another interpretation is that they play a central role in learning and memory. Anatomical studies suggest that arthropod mushroom bodies are predominately associated with olfactory pathways except in phylogenetically basal insects. The prominent olfactory input to the mushroom body calyces in more recent insect orders is an acquired character. An overview of the history of research on the mushroom bodies, as well as comparative and evolutionary considerations, provides a conceptual framework for discussing the roles of these neuropils.

The Organization of Extrinsic Neurons and Their Implications in the Functional Roles of the Mushroom Bodies in Drosophila melanogaster Meigen

Abstract: Although the importance of the Drosophila mushroom body in olfactory learning and memory has been stressed, virtually nothing is known about the brain regions to which it is connected. Using Golgi and GAL4–UAS techniques, we performed the first systematic attempt to reveal the anatomy of its extrinsic neurons. A novel presynaptic reporter construct, UAS-neuronal synaptobrevin–green fluorescent protein (n-syb–GFP), was used to reveal the direction of information in the GAL4-labeled neurons. Our results showed that the main target of the output neurons from the mushroom body lobes is the anterior part of the inferior medial, superior medial, and superior lateral protocerebrum. The lobes also receive afferents from these neuropils. The lack of major output projections directly to the deutocerebrum’s premotor pathways discourages the view that the role of the mushroom body may be that of an immediate modifier of behavior. Our data, as well as a critical evaluation of the literature, suggest that the mushroom body may not by itself be a “center” for learning and memory, but that it can equally be considered as a preprocessor of olfactory signals en route to “higher” protocerebral regions.

Mushroom bodies of the cockroach: their participation in place memory.

Abstract: Insects and other arthropods use visual landmarks to remember the location of their nest, or its equivalent. However, so far, only olfactory learning and memory have been claimed to be mediated by any particular brain region, notably the mushroom bodies. Here we describe the results of experiments that demonstrate that the mushroom bodies of the cockroach (Periplaneta americana), already shown to be involved in multimodal sensory processing, play a crucial role in place memory. Behavioral tests, based on paradigms similar to those originally used to demonstrate place memory in rats, demonstrate a rapid improvement in the ability of individual cockroaches to locate a hidden target when its position is provided by distant visual cues. Bilateral lesions of selected areas of the mushroom bodies abolish this ability but leave unimpaired the ability to locate a visible target. The present results demonstrate that the integrity of the pedunculus and medial lobe of a single mushroom body is required for place memory. The results are comparable to the results obtained from hippocampal lesions in rats and are relevant to recent studies on the effects of ablations of Drosophila mushroom bodies on locomotion. J. Comp. Neurol. 402:520–537, 1998. © 1998 Wiley-Liss, Inc.

Crustacean-insect relationships: the use of brain characters to derive phylogeny amongst segmented invertebrates.

Abstract: Conserved neural characters identified in the brains of a variety of segmented invertebrates and outgroups have been used to reconstruct phylogenetic relationships. The analysis suggests that insects

Mushroom bodies of the cockroach: Activity and identities of neurons recorded in freely moving animals

Abstract: This article describes novel attributes of the mushroom bodies of cockroaches revealed by recording from neurons in freely moving insects. The results suggest several hitherto unrecognized functions of the mushroom bodies: extrinsic neurons that discriminate between imposed and self-generated sensory stimulation, extrinsic neurons that monitor motor actions, and a third class of extrinsic neurons that predict episodes of locomotion and modulate their activity depending on the turning direction. Electrophysiological units have been correlated with neurons that were partially stained by uptake of copper ions and silver intensification. Neurons so revealed correspond to Golgi-impregnated or Lucifer yellow-filled neurons and demonstrate that their processes generally ascend to other areas of the protocerebrum. The present results support the idea of multiple roles for the mushroom bodies. These include sensory discrimination, the integration of sensory perception with motor actions, and, as described in the companion article, a role in place memory. J. Comp.

Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly

Abstract: In dipteran insects, the lobula plate neuropil provides a major efferent supply to the premotor descending neurons that control stabilized flight. The lobula plate itself is supplied by two major parallel retinotopic pathways from the medulla: small-field, magnocellular afferents that are implicated in achromatic motion processing and Y cells that connect the medulla with both the lobula plate and the lobula. A third pathway from the medulla involves transmedullary (Tm) neurons, which provide inputs to palisades of small-field neurons in the lobula. Although, in their passage to the brain, many output neurons from the lobula plate are separated physically from their counterparts in the lobula, there is an additional class of lobula complex output neurons. This group is composed of retinotopic lobula plate-lobula (LPL) and lobula-lobula plate (LLP) cells, each of which has dendrites in both the lobula and the lobula plate. The present account describes the anatomy and physiology of exemplars of LPL and LLP neurons, a wide-field tangential neuron that is intrinsic to the lobula complex, and representatives of the Tm- and Y-cell pathways. We demonstrate novel features of the lobula plate, which previously has been known as a motion-collating neuropil, and now also can be recognized as supporting direction- or nondirection-specific responses to local motion, encoding of contrast frequency, and processing of local structural features of the visual panorama. J. Comp. Neurol. 396:84–104, 1998. © 1998 Wiley-Liss, Inc.