scholarly journals Brain composition in Heliconius butterflies, post-eclosion growth and experience dependent neuropil plasticity

2015 ◽  
Author(s):  
Stephen H Montgomery ◽  
Richard M Merrill ◽  
Swidbert R Ott

Behavioral and sensory adaptations are often based in the differential expansion of brain components. These volumetric differences represent changes in investment, processing capacity and/or connectivity, and can be used to investigate functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here, we describe the brain composition of two species of Heliconius butterflies, a long-standing study system for investigating ecological adaptation and speciation. We confirm a previous report of striking mushroom body expansion, and explore patterns of post-eclosion growth and experience-dependent plasticity in neural development. This analysis uncovers age- and experience-dependent post-emergence mushroom body growth comparable to that in foraging hymenoptera, but also identifies plasticity in several other neuropil. An interspecific analysis indicates that Heliconius display remarkable levels of investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a useful case study in evolutionary neurobiology.

Physiology ◽  
2010 ◽  
Vol 25 (6) ◽  
pp. 338-346 ◽  
Author(s):  
Germain U. Busto ◽  
Isaac Cervantes-Sandoval ◽  
Ronald L. Davis

Studies of olfactory learning in Drosophila have provided key insights into the brain mechanisms underlying learning and memory. One type of olfactory learning, olfactory classical conditioning, consists of learning the contingency between an odor with an aversive or appetitive stimulus. This conditioning requires the activity of molecules that can integrate the two types of sensory information, the odorant as the conditioned stimulus and the aversive or appetitive stimulus as the unconditioned stimulus, in brain regions where the neural pathways for the two stimuli intersect. Compelling data indicate that a particular form of adenylyl cyclase functions as a molecular integrator of the sensory information in the mushroom body neurons. The neuronal pathway carrying the olfactory information from the antennal lobes to the mushroom body is well described. Accumulating data now show that some dopaminergic neurons provide information about aversive stimuli and octopaminergic neurons about appetitive stimuli to the mushroom body neurons. Inhibitory inputs from the GABAergic system appear to gate olfactory information to the mushroom bodies and thus control the ability to learn about odors. Emerging data obtained by functional imaging procedures indicate that distinct memory traces form in different brain regions and correlate with different phases of memory. The results from these and other experiments also indicate that cross talk between mushroom bodies and several other brain regions is critical for memory formation.


2021 ◽  
pp. jeb.238899
Author(s):  
Mallory A. Hagadorn ◽  
Makenna M. Johnson ◽  
Adam R. Smith ◽  
Marc A. Seid ◽  
Karen M. Kapheim

In social insects, changes in behavior are often accompanied by structural changes in the brain. This neuroplasticity may come with experience (experience-dependent) or age (experience-expectant). Yet, the evolutionary relationship between neuroplasticity and sociality is unclear, because we know little about neuroplasticity in the solitary relatives of social species. We used confocal microscopy to measure brain changes in response to age and experience in a solitary halictid bee (Nomia melanderi). First, we compared the volume of individual brain regions among newly-emerged females, laboratory females deprived of reproductive and foraging experience, and free-flying, nesting females. Experience, but not age, led to significant expansion of the mushroom bodies—higher-order processing centers associated with learning and memory. Next, we investigated how social experience influences neuroplasticity by comparing the brains of females kept in the laboratory either alone or paired with another female. Paired females had significantly larger olfactory regions of the mushroom bodies. Together, these experimental results indicate that experience-dependent neuroplasticity is common to both solitary and social taxa, whereas experience-expectant neuroplasticity may be an adaptation to life in a social colony. Further, neuroplasticity in response to social chemical signals may have facilitated the evolution of sociality.


BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
Ludwik Gąsiorowski ◽  
Aina Børve ◽  
Irina A. Cherneva ◽  
Andrea Orús-Alcalde ◽  
Andreas Hejnol

Abstract Background The brain anatomy in the clade Spiralia can vary from simple, commissural brains (e.g., gastrotrichs, rotifers) to rather complex, partitioned structures (e.g., in cephalopods and annelids). How often and in which lineages complex brains evolved still remains unclear. Nemerteans are a clade of worm-like spiralians, which possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been previously suggested as homologs to the annelid mushroom bodies. To understand the developmental and evolutionary origins of the complex brain in nemerteans and spiralians in general, we investigated details of the neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber. Results In the juveniles, the CNS is already composed of all major elements present in the adults, including the brain, paired longitudinal lateral nerve cords, and an unpaired dorsal nerve cord, which suggests that further neural development is mostly related with increase in the size but not in complexity. The ultrastructure of the juvenile cerebral organ revealed that it is composed of several distinct cell types present also in the adults. The 12 transcription factors commonly used as brain cell type markers in bilaterians show region-specific expression in the nemertean brain and divide the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, several of the mushroom body-specific genes are expressed in the developing cerebral organs. Conclusions The dissimilar expression of molecular brain markers between L. ruber and the annelid Platynereis dumerilii indicates that the complex brains present in those two species evolved convergently by independent expansions of non-homologous regions of a simpler brain present in their last common ancestor. Although the same genes are expressed in mushroom bodies and cerebral organs, their spatial expression within organs shows apparent differences between annelids and nemerteans, indicating convergent recruitment of the same genes into patterning of non-homologous organs or hint toward a more complicated evolutionary process, in which conserved and novel cell types contribute to the non-homologous structures.


2018 ◽  
Author(s):  
Jill R. Crittenden ◽  
Efthimios M. C. Skoulakis ◽  
Elliott. S. Goldstein ◽  
Ronald L. Davis

ABSTRACTMEF2 (myocyte enhancer factor 2) transcription factors are found in the brain and muscle of insects and vertebrates and are essential for the differentiation of multiple cell types. We show that in the fruitfly Drosophila, MEF2 is essential for normal development of wing veins, and for mushroom body formation in the brain. In embryos mutant for D-mef2, there was a striking reduction in the number of mushroom body neurons and their axon bundles were not detectable. D-MEF2 expression coincided with the formation of embryonic mushroom bodies and, in larvae, expression onset was confirmed to be in post-mitotic neurons. With a D-mef2 point mutation that disrupts nuclear localization, we find that D-MEF2 is restricted to a subset of Kenyon cells that project to the α/β, and γ axonal lobes of the mushroom bodies, but not to those forming the α’/β’ lobes. Our findings that ancestral mef2 is specifically important in dopamine-receptive neurons has broad implications for its function in mammalian neurocircuits.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Najia A Elkahlah ◽  
Jackson A Rogow ◽  
Maria Ahmed ◽  
E Josephine Clowney

In order to represent complex stimuli, principle neurons of associative learning regions receive combinatorial sensory inputs. Density of combinatorial innervation is theorized to determine the number of distinct stimuli that can be represented and distinguished from one another, with sparse innervation thought to optimize the complexity of representations in networks of limited size. How the convergence of combinatorial inputs to principle neurons of associative brain regions is established during development is unknown. Here, we explore the developmental patterning of sparse olfactory inputs to Kenyon cells of the Drosophila melanogaster mushroom body. By manipulating the ratio between pre- and post-synaptic cells, we find that postsynaptic Kenyon cells set convergence ratio: Kenyon cells produce fixed distributions of dendritic claws while presynaptic processes are plastic. Moreover, we show that sparse odor responses are preserved in mushroom bodies with reduced cellular repertoires, suggesting that developmental specification of convergence ratio allows functional robustness.


2009 ◽  
Vol 21 (11) ◽  
pp. 2217-2229 ◽  
Author(s):  
Jessica F. Cantlon ◽  
Melissa E. Libertus ◽  
Philippe Pinel ◽  
Stanislas Dehaene ◽  
Elizabeth M. Brannon ◽  
...  

As literate adults, we appreciate numerical values as abstract entities that can be represented by a numeral, a word, a number of lines on a scorecard, or a sequence of chimes from a clock. This abstract, notation-independent appreciation of numbers develops gradually over the first several years of life. Here, using functional magnetic resonance imaging, we examine the brain mechanisms that 6- and 7-year-old children and adults recruit to solve numerical comparisons across different notation systems. The data reveal that when young children compare numerical values in symbolic and nonsymbolic notations, they invoke the same network of brain regions as adults including occipito-temporal and parietal cortex. However, children also recruit inferior frontal cortex during these numerical tasks to a much greater degree than adults. Our data lend additional support to an emerging consensus from adult neuroimaging, nonhuman primate neurophysiology, and computational modeling studies that a core neural system integrates notation-independent numerical representations throughout development but, early in development, higher-order brain mechanisms mediate this process.


Zoomorphology ◽  
2021 ◽  
Author(s):  
Patrick Beckers ◽  
Carla Pein ◽  
Thomas Bartolomaeus

AbstractMushroom bodies are known from annelids and arthropods and were formerly assumed to argue for a close relationship of these two taxa. Since molecular phylogenies univocally show that both taxa belong to two different clades in the bilaterian tree, similarity must either result from convergent evolution or from transformation of an ancestral mushroom body. Any morphological differences in the ultrastructure and composition of mushroom bodies could thus indicate convergent evolution that results from similar functional constraints. We here study the ultrastructure of the mushroom bodies, the glomerular neuropil, glia-cells and the general anatomy of the nervous system in Sthenelais boa. The neuropil of the mushroom bodies is composed of densely packed, small diameter neurites that lack individual or clusterwise glia enwrapping. Neurites of other regions of the brain are much more prominent, are enwrapped by glia-cell processes and thus can be discriminated from the neuropil of the mushroom bodies. The same applies to the respective neuronal somata. The glomerular neuropil of insects and annelids is a region of higher synaptic activity that result in a spheroid appearance of these structures. However, while these structures are sharply delimited from the surrounding neuropil of the brain by glia enwrapping in insects, this is not the case in Sthenelais boa. Although superficially similar, there are anatomical differences in the arrangement of glia-cells in the mushroom bodies and the glomerular neuropil between insects and annelids. Hence, we suppose that the observed differences rather evolved convergently to solve similar functional constrains than by transforming an ancestral mushroom body design.


2021 ◽  
Author(s):  
Ludwik Gąsiorowski ◽  
Aina Børve ◽  
Irina A. Cherneva ◽  
Andrea Orús-Alcalde ◽  
Andreas Hejnol

AbstractBackgroundNemertea is a clade of worm-like animals, which belongs to a larger animal group called Spiralia (together with e.g. annelids, flatworms and mollusks). Many of the nemertean species possess a complex central nervous system (CNS) with a prominent brain, and elaborated chemosensory and neuroglandular cerebral organs, which have been suggested as homologues to the annelid mushroom bodies. In order to understand the developmental and evolutionary origins of complex nemertean brain, we investigated details of neuroanatomy and gene expression in the brain and cerebral organs of the juveniles of nemertean Lineus ruber.ResultsIn the hatched juveniles the CNS is already composed of all major elements present in the adults, including the brain (with dorsal and ventral lobes), paired longitudinal lateral nerve cords and an unpaired dorsal nerve cord. The TEM investigation of the juvenile cerebral organ revealed that the structure is already composed of several distinct cell types present also in the adults. We further investigated the expression of twelve transcription factors commonly used as brain and cell type markers in bilaterian brains, including genes specific for annelid mushroom bodies. The expression of the investigated genes in the brain is region-specific and divides the entire organ into several molecularly distinct areas, partially overlapping with the morphological compartments. Additionally, we detected expression of mushroom body specific genes in the developing cerebral organs.ConclusionsAt the moment of hatching, the juveniles of L. ruber already have a similar neuroarchitecture as adult worms, which suggests that further neural development is mostly related with increase in the size but not in complexity. Comparison in the gene expression between L. ruber and the annelid Platynereis dumerilii and other spiralians, indicates that the complex brains present in those two species evolved convergently by independent expansion of non-homologues regions of the simpler brain present in their common ancestor. The similarities in gene expression in mushroom bodies and cerebral organs might be a result of the convergent recruitment of the same genes into patterning of non-homologues organs or the results of more complicated evolutionary processes, in which conserved and novel cell types contribute to the non-homologues structures.


2020 ◽  
Author(s):  
Gonzalo H. Olivares ◽  
Franco Núñez ◽  
Noemi Candia ◽  
Karen Oróstica ◽  
Franco Vega-Macaya ◽  
...  

AbstractThe genetic variation of complex behaviors depends on the variation of brain structure and organization. The mechanisms by which the genome interacts with the nutritional environment during development to shape the brain and behaviors of adults are not well understood. Here we use the Drosophila Genetic Reference Panel to identify genes and pathways underlying this interaction in sleep behavior and mushroom bodies morphology.We identify genes associated with sleep sensitivity to early nutrition, from which protein networks responsible for translation, endocytosis regulation, ubiquitination, lipid metabolism, and neural development emerge. We confirm that genes regulating neural development and insulin signaling in mushroom bodies contribute to the variable response to nutrition. We propose that natural variation in genes that control the development of the brain interact with early-life malnutrition to contribute to variation of adult sleep behavior.


2019 ◽  
Author(s):  
Najia A. Elkahlah ◽  
Jackson A. Rogow ◽  
Maria Ahmed ◽  
E. Josephine Clowney

AbstractIn order to represent complex stimuli, principle neurons of associative learning regions receive combinatorial sensory inputs. Density of combinatorial innervation is theorized to determine the number of distinct stimuli that can be represented and distinguished from one another, with sparse innervation thought to optimize the complexity of representations in networks of limited size. How the convergence of combinatorial inputs to principle neurons of associative brain regions is established during development is unknown. Here, we explore the developmental patterning of sparse olfactory inputs to Kenyon cells of the Drosophila melanogaster mushroom body. By manipulating the ratio between pre- and post-synaptic cells, we find that postsynaptic Kenyon cells set convergence ratio: Kenyon cells produce fixed distributions of dendritic claws while presynaptic processes are plastic. Moreover, we show that sparse odor responses are preserved in mushroom bodies with reduced cellular repertoires, suggesting that developmental specification of convergence ratio allows functional robustness.


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