Central processing in the mushroom bodies
Introduction
The mushroom bodies are striking in appearance, resembling bilaterally arranged cups brimming with tiny neurons, supported by stems that bend and branch in several directions dorsally and laterally. The tiny neurons, Kenyon cells, (KCs) send long thin processes down through the stems, which form distinct lobes. These prominent and complex structures, found in all but the earliest insects, are as interesting as they look — they serve a number of functions important for processing sensory information. In many insects, groups of KCs receive sensory information from visual, gustatory, and mechanosensory areas, and, perhaps most often studied, thick tracts of olfactory input from the antennal lobes [1, 2]. In honeybees and other insects, different populations of KCs appear to receive direct input from different sensory modalities, although some KCs may also be multimodal. The KCs also receive inhibitory and recurrent input, and neuromodulators such as dopamine that provide reward signals [3]. Together, these inputs endow the mushroom bodies with information processing powers that are gradually coming to light. Here, focusing mainly on olfaction, I discuss functionally related roles the mushroom bodies appear to play in signal gain control, response sparsening, the separation of similar signals (decorrelation), and learning and memory.
Section snippets
Gain control
Sensory stimuli can be weak or strong, and sensory systems must accommodate this dynamic range. In several insect species the mushroom body's KCs have been found to form feedback connections with powerful inhibitory neurons that may help contain responses to sensory stimulus within limits (Figure 1). The anatomy of feedback connectivity provides a hint that any increase in the output of KCs will be tamped down by inhibition that increases proportionally with the response of the KCs, and is
Sparsening and decorrelation
Among the inputs received by KCs are olfactory signals carried by projection neurons from the antennal lobe. Anatomical studies show that each olfactory KC receives input from multiple presynaptic projection neurons [6, 7], and electrophysiological recordings show that the projection neurons (PNs), which are spontaneously active in the absence of stimuli [8], respond to odors with voluble bursts of spikes. Given the sheer number of action potentials arriving at KCs, one might predict these
Learning and memory
The mushroom bodies have long been associated with learning and memory. In numerous insect species, the volume of the mushroom body calyx has been shown to increase with sensory experience, not just with age (see [24] for several examples). Retrograde amnesia following olfactory training was induced in honeybees by specifically cooling the mushroom bodies [25], and honeybees treated early in life to develop without full mushroom bodies behaved quite normally as adults, but were deficient in
Reading the output of KCs
The processing taking place within KCs exerts its effects upon follower cells. In Drosophila, most of the neurons following from KCs have been identified and mapped [38], and their contributions to mushroom body function no doubt will soon be revealed. To date, though, work in other insects has provided interesting clues about how the output of KCs is processed by follower neurons. Recent work in the locust shows that the precise timing of the very sparse spikes elicited by odors in KCs carries
Conclusions: what the mushroom bodies are for
The mushroom body serves as a central processing unit within the insect brain. It receives sensory input from multiple modalities as well as modulatory signals reflecting internal state and external reward conditions; these modulators alter the properties and responses of the mushroom body's KCs and other neurons. The mushroom body combines and reformats the information it receives, projecting its volubly spiking input into sparse and well-separated representations. It excels at detecting
Acknowledgement
Many thanks to Dr. Kazumichi Shimizu for providing helpful comments on the manuscript.
References (41)
Writing memories with light-addressable reinforcement circuitry
Cell
(2009)- et al.
Encoding of olfactory information with oscillating neural assemblies
Science
(1994) - et al.
Functional analysis of a higher olfactory center, the lateral horn
J Neurosci
(2012) A pair of inhibitory neurons are required to sustain labile memory in the Drosophila mushroom body
Curr Biol
(2011)Different Kenyon cell populations drive learned approach and avoidance in Drosophila
Neuron
(2013)- et al.
Hebbian STDP in mushroom bodies facilitates the synchronous flow of olfactory information in locusts
Nature
(2007) - et al.
Conditional modulation of spike-timing-dependent plasticity for olfactory learning
Nature
(2012) Localization of a short-term memory in Drosophila
Science
(2000)- et al.
Limited taste discrimination in Drosophila
Proc Natl Acad Sci U S A
(2010) Normalization for sparse encoding of odors by a wide-field interneuron
Science
(2011)
Sparse, decorrelated odor coding in the mushroom body enhances learned odor discrimination
Nat Neurosci
A simple connectivity scheme for sparse coding in an olfactory system
J Neurosci
Olfactory representations by Drosophila mushroom body neurons
J Neurophysiol
Spontaneous olfactory receptor neuron activity determines follower cell response properties
J Neurosci
Odorant-induced oscillations in the mushroom bodies of the locust
J Neurosci
Imaging a population code for odor identity in the Drosophila mushroom body
J Neurosci
Intensity versus identity coding in an olfactory system
Neuron
Integration of the olfactory code across dendritic claws of single mushroom body neurons
Nat Neurosci
Intrinsic membrane properties and inhibitory synaptic input of kenyon cells as mechanisms for sparse coding?
J Neurophysiol
Impaired odour discrimination on desynchronization of odour-encoding neural assemblies
Nature
Cited by (31)
Genealogical relationships of mushroom bodies, hemiellipsoid bodies, and their afferent pathways in the brains of Pancrustacea: Recent progress and open questions
2021, Arthropod Structure and DevelopmentCitation Excerpt :In addition to olfactory input, hexapod mushroom bodies also receive highly processed gustatory, acoustic, visual, and mechanosensory input in a species-specific pattern and hence process multimodal sensory cues in the context of odor representation (Farris, 2005a; Galizia, 2008; Farris, 2011; Heuer et al., 2012; Strausfeld, 2012; Szyszka and Galizia, 2015). They were also shown to provide the neuronal substrate for olfactory memory formation and consolidation, multimodal learning, and place memory (Fahrbach, 2006; Farris, 2011; Martin et al., 2011; Heisenberg, 2014; Menzel, 2014; Stopfer, 2014; Menzel and Greggers, 2015; Wolff and Strausfeld, 2016). Research on the D. melanogaster MBs focusses, e. g., on their role in action selection, associative learning, the competing demands of rapid learning with long-term stability of memory, and forgetting (e.g., Modi et al., 2020; Baltruschat et al., 2021).
Influence of bio-inspired activity regulation through neural thresholds learning in the performance of neural networks
2021, NeurocomputingCitation Excerpt :The action of the GGN together with the oscillatory activity they receive from the PNs shape the activity of KCs in a cyclical way: KCs receive inputs from PNs and their activity increases, so that they are immediately inhibited by the action of the GGN. Therefore, the response in KCs can only occur in the period between successive inhibitions by the GGN [58,25]. In addition to all the previous, another important factor that helps sparse code to arise is that the ratio between the population of PNs and KCs in the locust is 1:50 [27,59].
Multi-regional circuits underlying visually guided decision-making in Drosophila
2020, Current Opinion in NeurobiologyCitation Excerpt :A third major pathway out of the optic lobes leads from the medulla, lobula, and accessory medulla directly [34,68,69] or through the PLP [69] to a higher-order area called the mushroom bodies (MBs). The MBs are well-studied for their role in learning and memory, particularly for olfactory input [70]. Anatomical studies suggest the MBs may also perform specific multisensory integrations, as input from visual, olfactory and gustatory processing converge in different combinations on the three MB lobes [34].
Crustacean olfactory systems: A comparative review and a crustacean perspective on olfaction in insects
2018, Progress in NeurobiologyCitation Excerpt :In insect mushroom bodies, the projection neurons synapse onto a large number of Kenyon cells, as many as 180,000 in bees and 175,000 in cockroaches (Galizia, 2008), numbers that are close to those of local interneurons associated with the comparable malacostracan protocerebral centers (Krieger et al., 2010). The PN axons terminate perpendicularly to arrays of Kenyon cells to establish a matrix of synaptic connections, an array that may promote a combinatorial readout across projection neurons (Figs. 13 and 14; reviewed e.g. in Fahrbach, 2006; Farris, 2005, 2011; Galizia, 2008; Martin et al., 2011; Strausfeld, 2009, 2012; Stopfer, 2014; Wolff and Strausfeld, 2016). A similar geometrical layout involving a rectilinear arrangement of extrinsic and large numbers of small, intrinsic neurons (not equivalent to the crayfish parasol cells) has recently been discovered in the hemiellipsoid bodies of the terrestrial hermit crab C. clypeatus, although the gross morphology of these structures displays little similarities to insect mushroom bodies (Fig. 14; Wolff et al., 2012).
Unraveling the Neurobiology of Sleep and Sleep Disorders Using Drosophila
2017, Current Topics in Developmental Biology