Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences

doi:10.1016/0006-8993(80)91007-0

Brain Research

Volume 192, Issue 1, 16 June 1980, Pages 49-59

https://doi.org/10.1016/0006-8993(80)91007-0 Get rights and content

Summary

Using the rapid Golgi method, the morphology of dendritic spines was quantified in the calyxes of groups of newly emerged, nurse, and forager honeybees. These groups were studied because they represented distinct stages of behavioral development and cumulative experience which, according to recent vertebrate findings, may be associated with enlargement of the spine head and stem shortening. Measurements were made of spine density, overall spine length, stem length, maximum head width, and profile area using eyepiece micrometry and computer image analyses. The results indicated that none of the groups differed appreciably in spine density and overall spine length. Foragers did exhibit spines with markedly larger profile areas and shorter stems than those in newly emerged and nurse honeybees. However, nurses and foragers did not differ appreciably in spine head width, but both groups had markedly wider heads than the newly emerged group did. These findings suggest that elongated growth of the spine head and concomitant stem shortening is an incremental process affecting different portions of the spine population at different rates. In particular, the growth rate of most spines appears to accelerate during the foraging stage in which the diversity of sensory stimulation is greatest.

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This review focuses on the neurobiological perspective. Changes in the morphology of Kenyon cell dendritic spines in association with orientation flights and foraging in honey bees (Apis mellifera) provided early evidence of MB plasticity [12,13]. In the 1990s, analyses based on the Cavalieri Principle were used to estimate regional brain volumes in honey bees.
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In the insect brain, mushroom bodies represent a prominent central neuropil for multisensory integration and, crucially, for learning and memory. For this reason, special attention has been focused on its small chemical synapses. Early studies on synaptic types and their distribution, using conventional electron microscopy, and recent publications have resolved basic features of synaptic circuits.
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Strangely, this axon is lost while auditory behavior remains active, so the consequence of its loss is not clear. Age-related changes in spine synapse morphology on the dendrites of spiny Kenyon cells in the brains of worker honeybees (Coss et al., 1980) are somewhat reminiscent of changes seen in spines in the ageing vertebrate forebrain. As noted above, the ageing forebrain, especially the frontal cortex, can show a loss of thin spines in favor of short, thick, mushroom-like ones.
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The neuropils associated with the mushroom bodies are significantly larger in more experienced foragers than in less experienced foragers (Durst et al., 1994; Withers et al., 1993). Foraging experience has also been linked to changes in mushroom body dendritic spine morphology and to changes in the number and volume of areas of synaptic contact in the calyces of the mushroom bodies called microglomeruli (Coss et al., 1980; Krofczik et al., 2008). Studies of precocious foragers indicated that the changes in the mushroom body neuropils reflect primarily foraging experience rather than age (Farris et al., 2001; Withers et al., 1993).
Foraging experience is correlated with structural plasticity of the mushroom bodies of the honey bee brain. While several neurotransmitter and intracellular signaling pathways have been previously implicated as mediators of these structural changes, none interact directly with the cytoskeleton, the ultimate effector of changes in neuronal morphology. The Rho family of GTPases are small, monomeric G proteins that, when activated, initiate a signaling cascade that reorganizes the neuronal cytoskeleton. In this study, we measured activity of two members of the Rho family of GTPases, Rac and RhoA, in the mushroom bodies of bees with different durations of foraging experience. A transient increase in Rac activity coupled with a transient decrease in RhoA activity was found in honey bees with 4 days foraging experience compared with same-aged new foragers. These observations are in accord with previous reports based on studies of other species of a growth supporting role for Rac and a growth opposing role for RhoA. This is the first report of Rho GTPase activation in the honey bee brain.
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Spine enlargement has been known to occur primarily in small spines transforming them into larger spines (Matsuzaki et al., 2004) thereby effecting spine turnover (Trachtenberg et al., 2002). Spines are known to undergo experience-dependent morphological plasticity during adulthood (Chang and Greenough, 1984; Connor et al., 1980; Desmond and Levy, 1986; Trachtenberg et al., 2002; Holtmaat et al., 2005; Hofer et al., 2006, 2009; Jasińska et al., 2006, 2010; Goshen et al., 2009) and following social stimulation (Coss et al., 1980). This may be because of a correlation between spine dimensions and calcium concentrations in spine heads, important in the phosphorylation of synaptic proteins that is necessary for long-term synaptic plasticity (review Segal, 2005).
Environmental enrichment paradigms in adult laboratory animals, consisting of physical, perceptual, and social stimulation, have been shown to affect synapse and cell morphology in sensory cortex and enhance learning ability, whereas enrichment, which is in harmony with the animal's natural habitat may have even greater implications for plasticity. Previous studies in our laboratory have shown that whisker stimulation induced the formation of synapses and spines in the corresponding barrel. In the present study adult C57/Bl6J female laboratory mice at 6 weeks of age were placed during 2 months in a protected enrichment enclosure in a forest clearing at the Chisti Les Biological Station, Tvier, Russia. We analyzed neuropil ultrastructure in the C2 barrel using serial-section electron microscopy on a total of eight mice (n=4 enriched, n=4 standard cagemate controls). Quantitative analyses of volumes of neuropil showed a significant increase in excitatory and inhibitory synapses on spines and excitatory synapses on dendritic shafts in the C2 barrel in the enriched group compared with standard cagemate controls. These results demonstrate that naturalistic experience alters the synaptic circuitry in layer IV of the somatosensory cortex, the first cortical relay of sensory information, leaving a lasting trace that may guide subsequent behavior.
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Three previous studies have directly examined spine density on dendrites of honey bee Kenyon cells (Coss et al., 1980; Brandon and Coss, 1982; Farris et al., 2001). Our study differs from these earlier studies in that we examined the density of spines in three distinct regions (proximal, medial, and distal with respect to the primary neurite) of the dendritic field rather than pooling all spines visible in a single plane of focus (Coss et al., 1980; Brandon and Coss, 1982) or measuring a single region (which corresponds to our defined medial region; Farris et al., 2001). We found that, while manipulation of muscarinic signaling did not affect total spine density, the distal region always had nearly twice as many total spines as either the proximal or medial regions.
The experience of foraging under natural conditions increases the volume of mushroom body neuropil in worker honey bees. A comparable increase in neuropil volume results from treatment of worker honey bees with pilocarpine, an agonist for muscarinic-type cholinergic receptors. A component of the neuropil growth induced by foraging experience is growth of dendrites in the collar region of the calyces. We show here, via analysis of Golgi-impregnated collar Kenyon cells with wedge arborizations, that significant increases in standard measures of dendritic complexity were also found in worker honey bees treated with pilocarpine. This result suggests that signaling via muscarinic-type receptors promotes the increase in Kenyon cell dendritic complexity associated with foraging. Treatment of worker honey bees with scopolamine, a muscarinic inhibitor, inhibited some aspects of dendritic growth. Spine density on the Kenyon cell dendrites varied with sampling location, with the distal portion of the dendritic field having greater total spine density than either the proximal or medial section. This observation may be functionally significant because of the stratified organization of projections from visual centers to the dendritic arborizations of the collar Kenyon cells. Pilocarpine treatment had no effect on the distribution of spines on dendrites of the collar Kenyon cells.

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Changes in morphology of dendritic spines on honeybee calycal interneurons associated with cumulative nursing and foraging experiences

Summary

Brain Research

Brain Research

Brain Research

Brain Research

Exp. Neurol.

A model for landmark learning in the honey-bee

J. comp. Physiol.

Structural and functional changes in an identified cricket neuron after separation from the soma, I. Structural changes

J. comp. Neurol.

Spine stems on tectal interneurons in jewel fish are shortened by social stimulation

Science

Visual interneurons in the median protocerebrum of the bee

J. comp. Physiol.

Ultrastructural changes in the dentate molecular layer during conditioning

Neurosci. Abstr.

Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area

J. Neurocytol.

Changes in dendritic spines of the dentate molecular layer during conditioning

Neurosci. Abstr.

Effects of dark rearing on dendritic spines in layer IV of the mouse visual cortex. A quantitative electron microscopial study

J. Anat. (Lond.)

Aberrant development of the Purkinje cell dendritic spine

Advanc. Neurol.

Neural integration (central nervous system)

Electric Current Flow in Excitable Cells