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.

Fine structure of mushroom bodies and the brain in Sthenelais boa (Phyllodocida, Annelida)

“…In insects, these cells are called Kenyon-cells, in Annelida globulicells. Branches of the pedunculus, called lobes, often merge medially with the ones on the corresponding side (Bullock and Horridge 1965;Strausfeld et al 1998). Mushroom bodies are supposed to be association areas or higher brain regions which are involved in olfactory perception, memory and learning in insects (Strausfeld et al 1998;Wolff and Strausfeld 2015).…”

“…Branches of the pedunculus, called lobes, often merge medially with the ones on the corresponding side (Bullock and Horridge 1965;Strausfeld et al 1998). Mushroom bodies are supposed to be association areas or higher brain regions which are involved in olfactory perception, memory and learning in insects (Strausfeld et al 1998;Wolff and Strausfeld 2015). Detailed studies on the function of mushroom bodies of polychaetes are lacking, but recently their relation to chemosensory function was shown in the annelid Platynereis dumerilii (Audouin and Milne Edwards 1833) (Chartier et al 2018).…”

Effects of dorsal and ventral vertical lobe electrolytic lesions on spatial learning and locomotor activity in Sepia officinalis.

“…Indeed, Moser and Moser (1998) reviewed anatomical and behavioral evidence for functional differentiation between the dorsal (locomotor activity) and ventral (spatial memory) parts of the hippocampus. Other studies have revealed functional subdivisions of mushroom bodies in arthropods (for a review, see Strausfeld et al, 1998; Yang, Armstrong, Vilinsky, Strausfeld, & Kaiser, 1995). The hippocampus in vertebrates and the VL in cephalopods appear to be constituted in sequences of matrices sharing the same properties (for a review, see Young, 1991).…”

“…From an evolutionary and comparative standpoint, understanding the neural basis of different types of learning and memory across a wide range of taxa is essential. To this purpose, numerous neuroethological studies have been performed in invertebrates, particularly arthropods (for a review, see Strausfeld, Hansen, Li, Gomez, & Ito, 1998) and mollusks (e.g., Aplysia ; for a review, see Kandel, 2003). Given their relatively simple nervous systems, they provide powerful model systems for the study of neuronal substrates and cellular mechanisms underlying learning and memory processes.…”

Contextual memory reactivation modulates Ca2+-activity network state in a mushroom body-like center of the crab N. granulata

“…In a recent article 10 , the long-standing discussion regarding possible genealogical relationships between insect MBs and malacostracan crustacean hemiellipsoid bodies was renovated based on newly obtained data 2 , 11 – 13 . According to previous suggestions 10 , 11 , we hereafter use the term MBs for these high-order centers of the protocerebrum in crustaceans.…”