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One brain was used for sagittal sections and the other for coronal sections.

Edited by John H. Byrne

The cerebral and cerebellar extracts were prepared from a third animal. Sections were desiccated at room temperature 15 min before use. Cerebral and cerebellar homogenates were prepared according to the literature [ 24 , 25 ] with modifications. Two microliters of cerebral or cerebellar homogenates or working solution of standards were spotted in an Omni Slide Prosolia Inc.

Each homogenate or solution was analyzed in triplicate. Initially, spots were analyzed in the positive ion mode and were then subsequentely analyzed in the negative ion mode, which makes the images of the spots in the negative ion mode look splashed. Firefly v. The step size was 0. Analyses were performed in either the negative and or positive ion modes. The images were acquired with 75, resolution. The signals attributed to the neurotransmitters were accurately assigned with errors less than 2 ppm see Supporting Information for chemical structures and details.

The acetylation of choline was performed according to the literature [ 27 ] with slight modifications. One exception was the pioneering work on neurotransmitter imaging that used laser ablation electrospray ionization MS to image GABA and choline [ 17 ]. In this scenario, DESI-MSI could contribute by specifically circumventing the problem of isobaric low molecular weight interferences from the matrix.

Color bars were added to facilitate visualization of the ion peaks of interest. DESI-MSI of the spots of the standard solutions first line in each Panel , cerebellar extract second line in each Panel , and cerebral extract third line in each Panel. Scale bar: 2 mm. Sagittal k and coronal l adjacent rat brain slices stained using the Nissl protocol.

Scale bar: 5 mm. As far as we could check, no profiles of acetylcholine in coronal sections have been reported. High spatial resolution MALDI-MSI images of acetylcholine in a sagittal rat brain section have, however, been reported, which corroborate our findings and is in accordance with the extensive axonal arborization found in the cell bodies of the striatal cholinergic interneurons [ 15 ].

More recently, the use of a derivatization strategy to obtain MALDI improved images of GABA distribution that closely resemble the images shown here has been reported [ 15 , 16 ]. In these works, GABA MSI of sagittal rat brain sections revealed the prevalence of this neurotransmitter in the hypothalamus, midbrain, and basal forebrain. GABA predominates in the hypothalamus and is also important in the midbrain and basal forebrain and its substructures [ 15 , 37 ]. Choline is not a neurotransmitter but is a precursor for the synthesis of phosphatidylcholines PC , which comprises one-half of the total membrane lipid content.

The increase in cell proliferation and cell membrane synthesis during tumorigenesis is known to affect the choline metabolism. Three-dimensional profiles of choline and choline-containing compounds are commonly obtained by proton magnetic resonance spectroscopy 1 H-MRS and positron emission tomography PET to follow tumor progression [ 38 ].

Few studies have, however, described mapping of choline in rat brains. The first image for choline distribution in a rat brain used HRMS to resolve the isobaric ions from protonated GABA and choline so as to produce selective MSI but showed very diffuse images from a coronal rat brain section with a slight prevalence of choline in the basal region [ 17 ]. Sagittal MSI of choline was further collected in two additional MSI studies [ 14 , 39 ], but a discussion about the anatomical distribution of this metabolite in the brain sections was not provided.

Ionic suppression plays an important but not exclusive role in the intensity of the images generated. In the literature, MSI of aspartic acid and serine are also scarce. Serine derivatized with TAHS was found in the striatum in the coronal section and in the hypothalamus, thalamus, and cortex in the sagittal section [ 16 ].

We have shown that the more direct and simpler ambient DESI-MSI technique is also able to reveal the spatial distribution of neurotransmitters in rat brain slices. Clear and well-resolved images were obtained, whereas the use of a high-resolution mass spectrometer was shown to be essential in order to address isobars and to collect selective images.

When the present study was in the final stage of preparation, Bergman et al. Our study corroborates and extends these findings, describing a detailed spatial distribution of the above-mentioned neurotransmitters as well as of aspartate, serine, and dopamine in coronal and sagittal rat brain slices. As we have anticipated [ 23 ], these results enlarge the application of atmospheric pressure ionization techniques to the field of neuroscience.

The authors thank the reviewers for valuable suggestions. Skip to main content Skip to sections. Advertisement Hide. Download PDF. Research Article First Online: 04 October Open image in new window. Introduction In the human body, arguably the brain is of most fundamental importance because it controls thinking, feelings, and memories, and also our major actions and reactions. Brain Extracts Cerebral and cerebellar homogenates were prepared according to the literature [ 24 , 25 ] with modifications.

Spot Analysis Two microliters of cerebral or cerebellar homogenates or working solution of standards were spotted in an Omni Slide Prosolia Inc. Synthesis of Acetylcholine The acetylation of choline was performed according to the literature [ 27 ] with slight modifications. For that we used an equimolar mixture of standards. Fortunately, acetylcholine and choline are cationic species, making them readily ionized by DESI, resulting in the two more intense ion peaks.

Dopamine is a strong base, is easily protonated, and produces a strong ion peak. The concomitant detection of all of these molecules in the mixtures of standards and in the extracts was observed. The abundance of choline is also notably larger in the extracts than in the mixture of the standards, which may occur because of better ionization of choline in the spots of the extracts due to low ionic suppression exerted by the other analytes, as by acetylcholine in particular.

The increase in the concentration of choline during the preparation of the extracts may also exacerbate this effect [ 33 ]. An advantage of avoiding derivatization agents is the possibility of imaging a broad range of molecules under the same conditions or in the same tissue slices while avoiding the risk of ion suppression or interfering side reactions [ 34 ].

These images show greater relative abundance of this neurotransmitter in the striatum, thalamus, and midbrain. Despite the relatively high concentration of cholinergic neurons in the brain, acetylcholine has been mapped only indirectly via its receptors or by enzymes related to their synthesis or degradation [ 15 ]. This MALDI-MSI distribution was corroborated by the intraperitoneal administration of tacrine, a central cholinesterase inhibitor that evoked a 7-fold increase in the concentration of acetylcholine-enriched regions [ 15 ].

Few MSI studies for rat brain slices monitoring this neurotransmitter have been reported. The results from both of these MSI studies are in good agreement with the images reported herein. Raichle, M. Merighi, A. Manuel, I. ACS Chem. Gessel, M. Wu, C. Mass Spectrom. Tata, A. Gemperline, E. Because aggregation can increase competition for local resources, the likelihood of conspecific aggression may also increase.

How is the shift from tolerance of conspecifics to aggression achieved? Key molecular players that drive or reinforce a new behavioral state include transcription factors, pheromonal receptors, biogenic amines, altered second messenger signaling, and neurotransmitters. A Examining the regulation of external information that drives aggregation versus aggressive behavior can be considered in a linear manner. B Understanding behavioral choice at the individual and population levels may occur as a result of a dynamic behavioral transition rather than a defined set point.

One key aspect of implementing a new behavioral state is flexibility in gene expression. Epigenetic mechanisms, including chromatin remodeling and DNA methylation, alter gene activity and are responsive to external pressures. Proteins containing a methyl-CpG-binding domain MBD bind methylated DNA and play a major role in determining the transcriptional state of the genome by coordinating crosstalk between DNA methylation, histone modifications, and chromatin organization Marhold et al. Hypermethylation of the male OA neurons genome also resulted in a decrease in male aggression; however, male—male courtship was not altered Gupta et al.

Neurons expressing this particular amine were analyzed because previous results demonstrated a subset of OA neurons directly receive male pheromone information and function to promote aggression Hoyer et al. These results suggest epigenetic mechanisms interpreted by MBD proteins are required for male social behavior and offer a specific neuronal genome to examine how potential shifts in gene expression, due at least in part in response to sensory stimuli, are coordinated at the epigenome level.

A second layer of gene expression control is through gene-specific transcription factors that often interact with cofactors to activate or repress expression. Transcription factors can function to control neuronal developmental processes that lead to alterations in behavior, regulate behavior itself due to the control of neuron function, or use a combination of developmental and behavioral processes. Work by the Dierick group has demonstrated that reducing the expression of the conserved Drosophila transcriptional repressor, tailless tll , results in a strong increase in male aggression Davis et al.

To confirm the increase in fighting frequency was independent of developmental defects, the authors reduced tll expression only in the adult and found the adult knockdown is sufficient to increase aggression. What target genes might Tll and its corepressor Atrophin regulate? One possible underlying mechanism that may be repressed is neuropeptide function because blocking neuropeptide processing or release suppresses the tll knockdown-induced aggression response Davis et al.

Too much or too little of the neuromodulator OA alters both aggression and mating behavior in numerous insects. Recent work has identified a specific transcription factor required to regulate the enzymatic production necessary for the synthesis of OA. By asking if alterations in Tfap-2 expression, specifically in OA neurons, effected Drosophila male aggression, Williams et al. The transcript levels of the vesicular monoamine transporter Vmat , which transports amines into synaptic vesicles, was also significantly reduced by a reduction in TfAP-2 and increased by TfAP-2 overexpression Williams et al.

Finally, a link between OA signaling and the satiation hormone Dsk was proposed, suggesting the internal nutritional state and external food-related chemical information may be ultimate targets of this molecular mechanism. Up to this point, controlling gene expression required for the function of neurons that may at least in part receive sensory information has been the focus. However, recent work has identified receptors that respond to aggression-promoting pheromonal information.

From a distance, cVA works as an aggregation pheromone Bartelt et al. How might the aggregation and the aggression-promoting effect of cVA be received by a male? In turn, cVA-promoted aggression can promote male fly dispersal from a food resource, in a manner dependent on Or67d-expressing sensory neurons. These data suggest that cVA may provide feedback information on male population density, through its effect on aggression.

However, long-term exposure to cVA may p. In the adult nervous system, neurotransmitters released from presynaptic terminals bind to receptors on postsynaptic cells, which lead to either an excitation or inhibition of these neurons. However, during nervous system development, neurotransmitters-neuromodulators, their synthesizing enzymes, and their receptors are often expressed before synapses are being formed Murrin et al. This autoregulatory mechanism might control the amount of OA released by octopamine neurons and regulate the structure of neuronal arborizations.

The presence of a positive feedback that controls the growth of modulatory inputs could provide a mechanism by which the experience of an animal can modify circuitry and subsequently potentially adapt to a changing environment Koon et al. One aspect of a dynamic environment repeatedly mentioned in this chapter is changing pheromonal information.

The existence of functional and synaptic connections between male pheromone responsive Gr32a neurons and OA neurons located in the subesophageal zone was recently demonstrated and the authors asked if Gr32a axonal morphology was altered when their synaptic partners lack OA Andrews et al. Using Gr32a-Gal4 to drive reporter GFP expression, the stereotypical projections of Gr32a-expressing neurons from control and OA-deficient males were examined.

Aberrant targeting of Gr32a axons in OA-deficient brains was observed, suggesting OA itself is required for the correct differentiation and positioning of OA neuron synapses targeted by pheromone-responsive sensory neurons. In modulating or strengthening a pheromonal or sensory signal, OA can be described as aggression promoting. However, in some insect societies, a signal to start aggressive behaviors must come at the expense of an ongoing behavior: cooperation.

When Polyrhachis moesta ant queens establish a colony with genetically unrelated queens, cooperative brood rearing and the exchange of food occur. These interactions are suggested to promote social partnership and can result in the transfer of hydrocarbons between nestmates, which is important in nestmate recognition Boulay et al. In contrast, colonies that contain a single queen exclude other queens via aggressive behavior. Koyama et al. Therefore, in this system, an OA-controlled increase in aggression may be considered a factor that reduces cooperation, and given that social cooperation needs to be continually reinforced by social bonding Boulay et al.

In invertebrates, amine neurons also project extensively throughout the brain Dacks et al. Amines are released and function, at least in part, via diffusion-mediated signaling, known as volume transmission Agnati et al.


Taking into account this complexity, are the multifaceted roles of biogenic amines in regard to social behavior separable? Recent work examining the role of a dopamine and the neuropeptide tachykinin receptor on aggression p. Their results indicate manipulating two distinct subsets of dopaminergic neurons resulted in an increase in male aggression Alekseyenko et al. Examining the presynaptic terminals of these aggression-promoting neurons within the T1 and PPM3 cluster revealed projections to different parts of the central complex a region of the Drosophila brain that is proposed to combine various modalities of sensory to direct behavioral responses , including regions that overlap with the receptor fields of DD2R and DopR DA receptor subtypes, respectively Alekseyenko et al.

These results suggest that specific DA neurons may influence aggression through direct or indirect communication with two distinct DA receptor subtypes. Aggression and courtship are two sexually dimorphic social behaviors. Tachykinin-expressing male-specific neurons that function in aggression have also been identified Asahina et al.

One theme in this review has been the role of sensory information in social behavior, and therefore it is striking that Tk neuron activation promotes aggression even in the absence of a variety of sensory cues Asahina et al. A second subset of male-specific aggression-promoting neurons was identified in a neuronal activation-based, large-scale screen in Drosophila. By expressing a genetically encoded far red-shifted channelrhodopsin CsChrimson reporter, the authors found P1 neuronal activation could promote aggression at a threshold below that required for a courtship behavioral pattern, the wing extension or song.

Decades of inquiry using invertebrates to examine the genetic and physiological mechanisms that regulate social behavior have provided exceptional contributions. These impacts have been felt on multiple levels; first, in regard to elucidating the principles required to wire behavior into the nervous system of any organism, and second, examining how insects behave has contributed to their management. The continued advancement of genetic-based tools and manipulations is moving the field of behavior forward not just in terms of neuronal communication but with questions concerning epigenetics and the integration of environmental influences.

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