Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee <i>Apis mellifera</i>

Haehnel, Melanie; Menzel, Randolf

doi:10.1242/jeb.059626

Cited by 31 publications

(19 citation statements)

References 58 publications

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“…GABAergic “feedback neurons” that connect subregions of the MB lobes and calyces, and whose processes in the lobes appear to be post-synaptic, are also been seen in other insects including honeybee or the moth Manduca , where there are about 50 or 150, respectively (Homberg et al, 1987; Grünewald, 1999a), rather than just one as in Drosophila . The honeybee feedback neurons respond to various sensory stimuli via input from the MB lobes, and their activity can be influenced by learning (Grünewald, 1999b; Haehnel and Menzel, 2010, 2012). …”

Section: Discussionmentioning

confidence: 99%

A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila

Masuda-Nakagawa¹,

Ito²,

Awasaki³

et al. 2014

Front. Neural Circuits

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Inhibition has a central role in defining the selectivity of the responses of higher order neurons to sensory stimuli. However, the circuit mechanisms of regulation of these responses by inhibitory neurons are still unclear. In Drosophila, the mushroom bodies (MBs) are necessary for olfactory memory, and by implication for the selectivity of learned responses to specific odors. To understand the circuitry of inhibition in the calyx (the input dendritic region) of the MBs, and its relationship with MB excitatory activity, we used the simple anatomy of the Drosophila larval olfactory system to identify any inhibitory inputs that could contribute to the selectivity of MB odor responses. We found that a single neuron accounts for all detectable GABA innervation in the calyx of the MBs, and that this neuron has pre-synaptic terminals in the calyx and post-synaptic branches in the MB lobes (output axonal area). We call this neuron the larval anterior paired lateral (APL) neuron, because of its similarity to the previously described adult APL neuron. Reconstitution of GFP partners (GRASP) suggests that the larval APL makes extensive contacts with the MB intrinsic neurons, Kenyon Cells (KCs), but few contacts with incoming projection neurons (PNs). Using calcium imaging of neuronal activity in live larvae, we show that the larval APL responds to odors, in a mannner that requires output from KCs. Our data suggest that the larval APL is the sole GABAergic neuron that innervates the MB input region and carries inhibitory feedback from the MB output region, consistent with a role in modulating the olfactory selectivity of MB neurons.

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Section: Discussionmentioning

confidence: 99%

A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila

Masuda-Nakagawa¹,

Ito²,

Awasaki³

et al. 2014

Front. Neural Circuits

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“…The MB is known to be involved in learning, memory formation, and memory retrieval in the honeybee (Menzel et al, 2006) and Drosophila (Davis, 2011), and it can be expected that extrinsic neurons provide a readout of the learned induced neural restructuring within the MB. The MB ␤ neurons have been recorded several times in the past and were found to change their response properties during olfactory conditioning (Mauelshagen, 1993;Grunewald, 1999;Okada et al, 2007;Haehnel andMenzel, 2010, 2012;Strube-Bloss et al, 2011). Simple differential conditioning experiments uncovered several associative phenomena.…”

Section: Discussionmentioning

confidence: 99%

Mushroom Body Extrinsic Neurons in the Honeybee Brain Encode Cues and Contexts Differently

Menzel

2013

J. Neurosci.

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Free-flying honeybees (Apis mellifera carnica) are known to learn the context to solve discrimination tasks. Here we apply classical conditioning of the proboscis extension response in restrained bees in combination with single-unit extracellular recordings from mushroom body (MB) extrinsic neurons elucidating the neural correlates of context-dependent olfactory discrimination. The contexts were light, colors, and temperatures, either alone or in combination. We found that bees learn context rules quickly and use them for better discrimination. They also solved a transwitching and a cue/context reversal task. Neurons extrinsic to the ␣ lobe of the MB reduced the responses to the rewarded odor, whereas they increased their responses to the context. These results indicate that MB extrinsic neurons encode cues and contexts differently. Data are discussed with reference to MB function.

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“…Recent studies on MBONs (receiving convergent inputs from many KCs) have revealed important insights on information processing properties of MB such as multisensory convergence, temporal coding properties, learning-induced changes in MBON activity and stimulus categorization by multisensory MBONs [106,109,110]. Intracellular recordings from individual neurons within a specific group of GABAergic feedback neurons (A3 PCT neurons, a specific group of MBONs forming recurrent circuits from the MB lobes to the MB-calyx input) has highlighted the role of these neurons in mediating memory-related changes from the MB output to the MB-calyx input [22,58,59,93,111]. Physiological recordings from KCs, so far, have been mostly limited to the calcium imaging of spatial activation patterns, which has revealed important insights into experience-related changes in spatial activation patterns of pre-and postsynaptic elements in MB-calyx MG [21,23,112].…”

Section: New Approaches and Methodological Advancesmentioning

confidence: 99%

Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

Groh

Rößler

2020

Insects

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Mushroom bodies (MBs) are multisensory integration centers in the insect brain involved in learning and memory formation. In the honeybee, the main sensory input region (calyx) of MBs is comparatively large and receives input from mainly olfactory and visual senses, but also from gustatory/tactile modalities. Behavioral plasticity following differential brood care, changes in sensory exposure or the formation of associative long-term memory (LTM) was shown to be associated with structural plasticity in synaptic microcircuits (microglomeruli) within olfactory and visual compartments of the MB calyx. In the same line, physiological studies have demonstrated that MB-calyx microcircuits change response properties after associative learning. The aim of this review is to provide an update and synthesis of recent research on the plasticity of microcircuits in the MB calyx of the honeybee, specifically looking at the synaptic connectivity between sensory projection neurons (PNs) and MB intrinsic neurons (Kenyon cells). We focus on the honeybee as a favorable experimental insect for studying neuronal mechanisms underlying complex social behavior, but also compare it with other insect species for certain aspects. This review concludes by highlighting open questions and promising routes for future research aimed at understanding the causal relationships between neuronal and behavioral plasticity in this charismatic social insect.

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Long-term memory and response generalization in mushroom body extrinsic neurons in the honeybee Apis mellifera

Cited by 31 publications

References 58 publications

A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila

A single GABAergic neuron mediates feedback of odor-evoked signals in the mushroom body of larval Drosophila

Mushroom Body Extrinsic Neurons in the Honeybee Brain Encode Cues and Contexts Differently

Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

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