Associative and Non-Associative Plasticity in Kenyon Cells of the Honeybee Mushroom Body

The insect mushroom bodies are higher-order brain centers and critical for odor learning. We investigated experience dependent plasticity of their intrinsic neurons, the Kenyon cells (KCs). Using calcium imaging, we recorded KC responses and investigated non-associative plasticity by applying repeated odor stimuli. Associative plasticity was examined by performing appetitive odor learning experiments. Olfactory, gustatory and tactile antennal stimuli evoked phasic calcium transients in sparse ensembles of responding KCs. Repeated stimulation with an odor led to a decrease in KCs' response strength. The pairing of an odor (conditioned stimulus, CS) with a sucrose reward (unconditioned stimulus) induced a prolongation of KC responses. After conditioning, KC responses to a rewarded odor (CS+) recovered from repetition-induced decrease, while the responses to a non-rewarded odor (CS−) decreased further. The spatio-temporal pattern of activated KCs changed for both odors when compared with the response before conditioning but the change was stronger for the CS−. These results demonstrate that KC responses are subject to non-associative plasticity during odor repetition and undergo associative plasticity after appetitive odor learning.

[1]  P. Mobbs.  The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies , 1982 .

[2]  M. Bitterman,et al.  Classical conditioning of proboscis extension in honeybees (Apis mellifera). , 1983, Journal of comparative psychology.

[3]  R. Rescorla.  Behavioral studies of Pavlovian conditioning. , 1988, Annual review of neuroscience.

[4]  G. Bicker,et al.  Habituation of an appetitive reflex in the honeybee. , 1992, Journal of neurophysiology.

[5]  R. Menzel,et al.  Anatomy of the mushroom bodies in the honey bee brain: The neuronal connections of the alpha‐lobe , 1993, The Journal of comparative neurology.

[6]  M. Hammer.  An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees , 1993, Nature.

[7]  J. Mauelshagen,et al.  Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. , 1993, Journal of neurophysiology.

[8]  M. Hammer,et al.  Food-induced arousal and nonassociative learning in honeybees: dependence of sensitization on the application site and duration of food stimulation. , 1994, Behavioral and neural biology.

[9]  M. Hammer.  The neural basis of associative reward learning in honeybees , 1997, Trends in Neurosciences.

[10]  M. Hammer,et al.  Backward inhibitory learning in honeybees: a behavioral analysis of reinforcement processing. , 1998, Learning & memory.

[11]  M. Hammer,et al.  Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. , 1998, Learning & memory.

[12]  S. Oleskevich,et al.  Cholinergic synaptic transmission in insect mushroom bodies in vitro. , 1999, Journal of neurophysiology.

[13]  G. Laurent,et al.  Short-term memory in olfactory network dynamics , 1999, Nature.

[14]  B. Grünewald,et al.  Morphology of feedback neurons in the mushroom body of the honeybee, Apis mellifera , 1999, The Journal of comparative neurology.

[15]  R. Menzel,et al.  Associative learning modifies neural representations of odors in the insect brain , 1999, Nature Neuroscience.

[16]  B. Grünewald,et al.  Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera , 1999, Journal of Comparative Physiology A.

[17]  R. Menzel,et al.  Nicotinic acetylcholine currents of cultured Kenyon cells from the mushroom bodies of the honey bee Apis mellifera , 1999, The Journal of physiology.

[18]  Randolf Menzel,et al.  Odour perception in honeybees: coding information in glomerular patterns , 2000, Current Opinion in Neurobiology.

[19]  R. Menzel,et al.  Visualizing mushroom body response to a conditioned odor in honeybees , 2001, Naturwissenschaften.

[20]  R. Menzel,et al.  GABA‐immunoreactive neurons in the mushroom bodies of the honeybee: An electron microscopic study , 2001, The Journal of comparative neurology.

[21]  N. Strausfeld.  Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes , 2002, The Journal of comparative neurology.

[22]  Glenn C. Turner,et al.  Oscillations and Sparsening of Odor Representations in the Mushroom Body , 2002, Science.

[23]  Uli Müller,et al.  Nitric Oxide/cGMP-Mediated Protein Kinase A Activation in the Antennal Lobes Plays an Important Role in Appetitive Reflex Habituation in the Honeybee , 2002, The Journal of Neuroscience.

[24]  B. Kimmerle,et al.  Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy , 2003, Journal of Comparative Physiology A.

[25]  Donald A. Wilson,et al.  Olfactory perceptual learning: the critical role of memory in odor discrimination , 2003, Neuroscience & Biobehavioral Reviews.

[26]  R. Menzel,et al.  Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes , 2003, Neuroscience.

[27]  M. Heisenberg.  Mushroom body memoir: from maps to models , 2003, Nature Reviews Neuroscience.

[28]  Karel Svoboda,et al.  Stereotyped Odor-Evoked Activity in the Mushroom Body of Drosophila Revealed by Green Fluorescent Protein-Based Ca2+ Imaging , 2004, The Journal of Neuroscience.

[29]  Ronald L. Davis,et al.  Olfactory Learning , 2004, Neuron.

[30]  C. Giovanni Galizia,et al.  Optical methods for analyzing odor-evoked activity in the insect brain , 2004 .

[31]  R. Menzel,et al.  Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. , 2005, Journal of neurophysiology.

[32]  A. Fiala,et al.  Punishment Prediction by Dopaminergic Neurons in Drosophila , 2005, Current Biology.

[33]  Gesine Bundrock,et al.  Focal and Temporal Release of Glutamate in the Mushroom Bodies Improves Olfactory Memory in Apis mellifera , 2005, The Journal of Neuroscience.

[34]  Ronald L. Davis,et al.  Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. , 2006, Neuron.

[35]  U. Müller,et al.  Memory , 2006, Cellular and Molecular Life Sciences CMLS.

[36]  Randolf Menzel,et al.  Dimensions of cognition in an insect, the honeybee. , 2006, Behavioral and cognitive neuroscience reviews.

[37]  R. Menzel,et al.  Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons , 2006, Journal of Comparative Physiology A.

[38]  Ronald L. Davis,et al.  Drosophila α/β Mushroom Body Neurons Form a Branch-Specific, Long-Term Cellular Memory Trace after Spaced Olfactory Conditioning , 2006, Neuron.

[39]  S. Waddell,et al.  Drosophila olfactory memory: single genes to complex neural circuits , 2007, Nature Reviews Neuroscience.

[40]  R. Menzel,et al.  Learning-Related Plasticity in PE1 and Other Mushroom Body-Extrinsic Neurons in the Honeybee Brain , 2007, The Journal of Neuroscience.

[41]  Edmund T Rolls,et al.  An attractor network in the hippocampus: theory and neurophysiology. , 2007, Learning & memory.

[42]  Andreas S. Thum,et al.  Behavioral/systems/cognitive Multiple Memory Traces for Olfactory Reward Learning in Drosophila Materials and Methods , 2022 .

[43]  Akira Mamiya,et al.  Imaging of an Early Memory Trace in the Drosophila Mushroom Body , 2008, The Journal of Neuroscience.