Measuring the effects of larval life stress on adult anxiety behavior in Drosophila melanogaster

Harjit Khaira, Trisha Trinidad, Jackson Luu, Shariq Khan, Noah Crockenberg
Department of Biology, Rutgers University, Camden, NJ. 08102


Anxiety  is  the  body’s  homeostatic  response  to  stressful situations. While anxiety is caused by factors such as pain, it has  been  categorized  as  a  response  that  helps  distinguish dangerous  situations.  Disruption  during  developmental stages directly affects an individual’s mental health and social behavior.  This  is  seen  in  the  offspring  of  pregnant  women when  exposed  to  famine  during  pregnancy,  resulting  in increased risks of coronary heart disease, diabetes, obesity, and other conditions. In this report we tested the hypothesis that Drosophila melanogaster that are frequently exposed to stress during early developmental stages will have amplified levels of anxiety as adults. This was conducted by using bright light  stress  stimuli  and  through  the  usage  of  optogenetics pain to cause anxiety like behavior in the flies. It was found that wild type Ore-R flies placed under stress stimuli as larvae showed  increased  anxiety  behavior  when  compared  to  the flies  that  were  not  exposed  to  stress  stimuli.  These  results confirm  that  stress  during  early  developmental  stages  can have severe behavioral effects later in life.


Anxiety is the body’s response to stressful situations. While anxiety may be caused by several factors, including pain, it has  been categorized  as  an  emotional  response  that  helps assess  dangerous  situations.  Anxiety-inducing  stimuli  in early  life  can  have  negative  effects  on  an  individual’s development (Mohammad et al., 2016). Disruption during the developmental stages directly affects an individual’s mental health  and  social  behavior.  Children  of  pregnant  women exposed  to  stresses  such  as  famine  during  pregnancy  are more susceptible to coronary heart disease, diabetes, obesity, microalbuminuria and accelerated cognitive aging as adults (Babenko et al., 2015). In Drosophila melanogaster, the effect of early life stress on late-stage anxiety behavior has yet to be studied.  This  behavioral  study  will  explore  if  exposure  to anxiety-inducing stimuli in early life will influence the levels of anxiety expressed in adult fruit flies. 
In  this  study,  we  assessed  anxiety  using  two  different behavioral  assays,  one  being  wall  following  assay  (WAFO) and  another  being  locomotive  assay,  which  are  both  well-established   anxiety   behavior   measurements   in D. melanogaster. Fruit flies are known to avoid the center of an area  due  to  distress  and  anxiety  which  is termed centrophobism   (Iliadi,2009).   By   taking   advantage of centrophobism,  the  wall  following  assay  was  developed where the flies under stressful or anxiety-inducing conditions show an increase in WAFO activity. They tend to cling to the walls of the arena more often than the non-anxious flies. The other measure of anxiety is the locomotive assay, where the decrease  of  locomotive  activity  is  an  indicator  of  anxiety behavior for fruit flies (Ostrowski et al., 2018). It has been proven  that  motivated  behavior,  such  as  walking,  can  be altered by induced stress. It was found that electric shock and high-temperature exposure over several minutes decreased flies’  walking  activity  that  lasted  around  eight  hours. Locomotive  activities  in D. melanogaster are  established  as the most direct way to assess anxiety behavior (Ostrowski et al., 2018).
There are several ways to induce anxiety in D. melanogaster which  includes  exposure  to  bright  light  stimuli  and  by optogenetic induction of pain. Bright light induces stress in Drosophila. Decreases   locomotor   activity   in   larvae, suggesting an increase in anxiety levels (Min and Condron, 2005).  Another  way  to  generate  anxiety  is  to  induce  pain through the usage of optogenetics. Optogenetics involves the genetic encoding of light-sensitive proteins called opsins, into cell membranes of neurons to allow for temporal control of cellular activity by photo-stimulation. There are many light-sensitive  opsins,  we  used  Chrimson,  a  red  light  sensitive opsin, to activate pain neurons as a way to induce anxiety in the animals in this study (Allsopet al., 2014).
In the current study, we examined whether anxiety-inducing stimuli during the developmental stages of D. melanogaster will  affect  late-stage  anxiety  behavioral  patterns.  We hypothesize that D. melanogaster that are frequently exposed to  stress  during  early  developmental  stages  will  have amplified levels of anxiety as adults.  It is known that animals exposed  to  stress  will  learn  to  avoid or  adapt  to  the phenomena that caused anxiety. There is evidence regarding changes  in  gene  expression  when  exposed  to  an anxiety stimulus (Sørensen et al., 2005). Another study explored the possible  relationship  between  prenatal  stress  exposure  in mammals to links to ADHD, schizophrenia, autism, anxiety, or depression later in life, and how epigenetic alterations have a large  influence  on  mental health  in  the  later  stages  of  life (Babenko et al., 2015). Here, we studied the effect of early life stress on Drosophila larvae on late stage anxiety behavior in the  adult  fruit  flies.  This  was  done  through  the  usage of optogenetic pain and bright light stress. Furthermore, their anxiety  behavior  was  assessed  through  locomotive  and WAFO assays.

Materials & Methods

D. melanogaster has been the model organism for extensively studying animal behavior and neurobiology. D. melanogaster works  well  as  a  model  organism  due  to  its  capability  to produce  large  amounts  of  progeny  during  its  short  eight-week  life  cycle.  Having  a  short  life  cycle  is  ideal  for  this behavioral  experiment  because  it  allows  for  adequate exposure of anxiety-inducing stimuli in the early larval stage and observation of anxiety-like behavior in the adult-stage.

Wild Type Flies

The Oregon-R wild type fruit flies used in the ongoing study were supplied by Dr. Kwangwon Lee’s laboratory at Rutgers-Camden  University.  The  stock was maintained  under  25-degree  Celsius,  in  cornmeal-based  fly  media,  in  which  they were allowed  to  breed  and  mature.  The  larvae  that  have hatched  in  the  media  will  be  used  for  experimental treatments. After the female fly lays eggs, it takes 24 hours for the larvae to hatch, after which they start to roam around the fly media. It was reported that D. melanogaster larvae mature into adult form in four to five days after female fruit flies lay the eggs (Stefan et al., 2012).

Larval Selection

There  are different  developmental  stages  of  larvae  forms, called instars. Larvae in the third instar stage were identified as  the  largest  of  larval  form,  and  were  utilized  for experimental treatments. Differentiation was made between 2nd and 3rd instars based off their spiracles. In the 2nd instar, the anterior spiracle is club-like, while in the 3rd instar it is branched. The posterior spiracles of the third instar also have a  dark  orange  ring  at  their  tip,  which  is  lacking  or  weakly present in the 2nd instar. This band was used to identify 3rd instars  when  they  are  feeding  and  only  their  posterior spiracles were visible. Larvae were then collected from the vials  using  a  Drosophila  sorting  brush  from  Carolina Biological, plastic handle, 6-½mm. They were then put into labeled 60mm x 15mm fisher brand stackable lid petri dishes for experimental treatments.

Optogenetics Flies

Optogenetic organisms 79598 opto ChR are highly sensitive to  the  light,  due  to  expression  of  the  light-sensitive  opsins proteins    (Guru    et    al.,    2015). Normally,    ChR (Channelrhodopsin-2) can induce an action potential in ChR expressing neurons through the usage of blue light. However, for   this   experiment   Chrimson   protein,   a   type   of channelrhodopsin  was  used,  which  gave  control  over  the activation  of  the  light  sensitive-ion  channel.  Chrimson  is  a fluorescent protein which is activated by red light instead of blue light. The main advantage of Chrimson is that we were able to use red light for stimulation without the worry of it being seen by the flies since they can not see red light. We expressed Chrimson only in pain neurons via the UAS-Gal4 system in ppk-GAL4/UAS-chrimson drosophila. Ppk is a gene only  expressed  in  class  4  sensory  neurons  which  are considered nociceptors. Class 4 sensory neurons are highly branched  multidendritic  sensory  neurons  in Drosophila larvae  that  function  as  nociceptors  that  are  necessary  for behavior responses to noxious mechanical stimuli (Zhong et al., 2010). Thus, our system will allow for specific activation of pain neurons as a way to induce anxiety in these animals.

The  optogenetic  strain  ppk-GAL4/UAS-chrimson  (79598) opto  ChR  received  from  the  Bloomington  Stock  Center  is  a Gal4/  UAS  system.  Gal4  is  a  transcription  factor  which activates transcription of its target genes by binding to UAS regulatory sites. In D. melanogaster, these two elements are carried in separate lines 32078 (encodes the ppk-gal4) and 55136  (encodes  the  UAS-Chrimson).  When  these  two  lines are crossed the progeny, 79598 opto ChR is expected to have Gal4 expressed in pain neurons. Due to this gene expression, red light exposure activates pain neurons. As a result, these flies  are  a  successful  model  organism  to  examine  anxiety behavior, since pain is known to cause anxiety (Allsop et al., 2014). Optogenetic stock cultivation and larvae identification was accomplished under the same protocol that was used to maintain Ore-R flies.


Two  types  of  stress-inducing  stimuli  were  being  given  to  the organisms  at  the  larval  stage  during  the  duration  of  the experiment. These stress stimuli included bright light for the wild type flies and then optogenetic pain for the optogenetic stock. In  a  previous  study,  it  was  found  that  bright  light causes anxiety in larvae due to their photophobic nature (Min and Condron, 2005). Because of the stress from light, larvae showed decreased locomotor activity. Hence, the reason why bright light was used to cause stress during the larval stage. The bright light source was provided by the Olympus SZX7 Stereo Microscope, the microscope uses LED lights which are of 1500 lumens.

Third instar larvae were placed in small 60mm x 15mm fisher brand stackable lid petri dish with 0.5ml of water to prevent them from desiccating during the exposure time. Then they were placed under a bright light for intervals of 10 minutes, 3 times for every 24 hours. Ten minutes of exposure time was chosen because it has shown to give the maximum behavior response in larvae (Min and Condron, 2005). The bright light stimuli were repeated until larvae initiate pupation. Near the enclosion stage of flies, the stimulus was stopped and they were allowed to mature into adults, which is the stage where their anxiety levels will be measured. 

For the 79598 opto ChR strain, the larvae were exposed to a red light instead of bright light. The red light was provided by a  LED  light  of  627  nm  wavelength,1100  lumens.  Red  light served  as  a  pain  activating  stressor  during  the  early developmental  stage,  due  to  Chrimson  being  expressed  in larval pain neurons. The same procedure that was used for wild type flies to induce stress will be followed. First, larvae were  placed  in  60mm  x  15mm  petri  dishes  with  0.5  ml  of water to prevent desiccation. Then they were placed under red  light  for  intervals  of  10  minutes,  3  times  for  every  24 hours  until  they  initiate  pupation.  Then  the  stimuli  were stopped, allowing the organisms to grow into adults, at which their anxiety levels will be measured.

Measurement of anxiety phenotype

The stress levels were measured by video recording the adult flies using an iPhone camera. The .mov format obtained from the  iPhone  recording  was  converted  to  .avi  since  it  is  the correct  format  the  fly  tracking  software  utilizes.  There  are multiple  analysis  programs  that  can  be  used  to  track D. melanogaster behavior. Such programs are: Ctrax, Biotrack, IDTracker, and Noldus Ethovision (Chao et al., 2015). In this experiment,  Ctrax  was  the  best  option  for  tracking  the organisms wall following behavior due to anxiety-inducing stimuli. The Ctrax software tracked the path traveled by each individual fly. First, the video was analyzed using the Ctrax software  which  then  will  produce  a  matLab  file  with  the position (x and y coordinates) of the fly in the arena. Then the positions of the flies were plotted, and the percentage of time spent along the wall was calculated. To quantify this, within 11 points from the left or right wall in the x coordinates was considered being along the wall, and 11 points within the top or  bottom  wall  in  the  y  coordinates  was  considered  being along  the  wall.  This  is  because  11  points  in  one  direction equated to approximately the length of a fruit fly.

In order to prepare the flies for video recording they were placed in a 40 × 40 mm 3-D printed square arena which is further  divided  into  4  chambers  resulting  in  20×20  mm chambers  with  a  height  of  1.5  mm. D.  melanogaster is considered centrophobic, like rodents, so they naturally tend to  cling  to  the  walls  of  the  container  they  are  kept in, especially when stressed (Iliadi, 2009). The intervals of time that the experimental flies stay near the walls of the square arena were being compared to the control. As a result, their time spent near the walls was utilized as an indicator of anxiety levels.

The  change  in  locomotion  behavior  and  the  time  the  flies spent  moving  in  the  square  arena  was  also  an  indicator  of anxiety. As a result, the time spend moving will be recorded the during a duration of 10-minute videos. Any change in the fly’s  displacement  was  considered  as  a  response.  It  was reported that the flies not exposed to previous stress tend to have more locomotive activity in an enclosed arena compared to flies exposed to stress, which show slow or no locomotive activities  at  all  (Ostrowskiet  al.,  2018).  A  t-test  was performed to examine the significant of values obtained from the stress and non-stressed groups. Where p-value <0.05 is considered statistically significant.

Experimental Plan

The experiment was conducted with four groups of flies: a control group of wild type Ore-R flies, a stress group of wild type  Ore-R  flies,  as  shown  in  Figure  1.  A  control  group  of optogenetic 79598 opto ChR flies, then finally a stress group of optogenetic79598 opto ChR flies. Every group was bred and their larvae were collected and separated into 60mm x 15mm  fisher  brand  stackable  lid  petri  dishes.  The  control group was allowed to grow into the adult phase without any stressors, and their behavior was observed via video tracking software  and  locomotive  assay.  The  larvae  from  the  stress group  of  wild  type  flies  were  put  under  stress  from  bright lights. They were exposed to bright light for 10 minutes, 3 times with 10-minute intervals in between, every 24 hours until  pupation.  When  they  reached  the  adult  phase,  their movements were also observed via video tracking software along with locomotive assay. The larvae from the optogenetic flies’ group were put under stress from a red light that caused them  to  feel pain,  which  will  induce  anxiety. They  were exposed to the red light for 10 minutes at a time, 3 times with 10-minute  intervals  in  between  every  24  hours  until pupation.  When  this  group  reached  the  adult  phase,  their movements were observed as well via tracking software and locomotive assay. 

Figure 1. Experimental design

Then, the amount of time each group of adult flies spent close to the walls were compared. This gave us an indication of the levels  of  anxiety  in  each  group.  From  this  data,  it  can be determined whether administering stress stimuli during the larvae  stage  of D. melanogaster will  amplify  anxiety  levels later in life. The locomotive assay also served as an indicator of stress, when the control no stress flies were compared to experimental stress flies.


Locomotive Assay of the Control and Stress Groups

To test if bright light during larval stage caused a locomotive change in adult life, we measured the flies time spent walking during  the  duration  of  10-minute  video  recordings.  It  was found  that  wild  type  Ore-R  stress  group  had  decreased locomotor activity compared to the wild type Ore-R control group (Fig. 2A). Ore-R stress groups locomotive behavior was statistically significant from that of the Ore-R stressed group (t-test, p-value: 0.0000823, p < 0.05, n=6). 

To  test  if  optogenetic  pain  during  larval  stage  caused locomotive change in adult life for 79598 opto ChR strain, the flies locomotive activities were also observed. In 79598 opto ChR,  the  opposite  trend  was  discovered  where  the  control group  displayed  decreased  locomotor  behavior  activities compared  to  the  stressed  group  which  showed  increase  in locomotor activities (Fig. 2B). However, optogenetic 79598 opto  ChR  stress  group  locomotive  behavior  was  not statistically  significant  from  that  of  the  79598  opto  ChR control group (t-test, p-value: 0.9390060, p > 0.05, n=6).

Figure 2.  A) Locomotive assay of control and stress group for wild type  Ore-R.  B) Locomotive  assay  of  control  and  stress  group  for 79598 optogenetic ChR flies.

Wall following (WAFO) of the Control and Stress Groups

In order to test if bright light stress stimuli will cause a change in wall following behavior (WAFO) compared to the control groups  in  Ore-R,  the  fly  movements  were  recorded  for  30 minutes. Then these were tracked by C-trax giving x and y coordinates of the flies positions. The x and y positions were plotted displaying their movements in the chambers (Fig. 3). In Figure 3A and 3B, the WAFO of the wild type control fly and stress fly can be visualized. Comparing the control fly versus the stress fly it can be observed that the control fly (Fig. 3A)moved the whole area of the arena. While the stress fly (Fig. 3B)  only  tracked  along  the  walls  of  the  arena.  Then  to quantitatively assess this observation, the percentage of time spent  moving  along  the  walls  of  the  arena  were  found.  In comparing Ore-R control and stress group, it was found that Ore-R control group was not statistically significant from that of stress group (t-test, p-value: 0.142854, n=4) (Fig. 3C).

Figure  3.  A)  Shows  the  x  and  y  coordinates  of  WAFO  activities obtained by C-trax of the no stress control Wild type Ore-R fly. B) Shows the x and y coordinates of WAFO activities of the stress Wild type Ore-R fly. C) Quantitatively assesses the WAFO behavior of n=4 flies  by  calculating  the  time  spent  near  the  wall  in  a  20×20  mm chamber, for control and stress flies.

Then  to  test  if  the  optogenetic  pain for  ChR  flies  caused  a change in WAFO behavior in control and stress group, their movements were also tracked by C-trax for a duration of 30 minutes. Figure 4A and 4B displays the WAFO movement of a ChR fly. In this case,it can be observed that the control fly (Fig. 4A) moved the whole area of the arena, however it do not have a clear wall following pattern while on the other hand the stress fly (Fig. 4B) shows a very defined tracking along the walls and the whole area of the arena.  Qunantivally, similar observation was seen in the optogenetic flies as in wild type, where the control group was not statistically significant from that of the stress group (t-test, p-value: 0.137332, p > 0.05, n=4) (Fig. 2D). However, there was a trend present where the WAFO activity of the stress group was higher than that of the control group for both Ore-R and the 79598 opto ChR strains.

Figure  4.  A)  Shows  the  x  and  y  coordinates  of  WAFO  activities obtained by C-trax of the no stress control 79598 opto ChR fly. B) Shows the x and y coordinates of WAFO activities of the stress 79598 opto ChR. C) Quantitatively assesses the WAFO behavior of n=4 flies by calculating the time spent near the wall in a 20×20 mm chamber, for control and stress flies.


Our  study  demonstrates  that  early  life  stress  can  induce anxiety-like behavior later in life. This confirms that exposure to bright light as larvae can inherently induce higher levels of anxiety  as  adults  in  Wild  type  Ore-R  strain,  as  seen  in the locomotive assay. This means the wild type flies serve as a successful model to measure the effect of anxiety behaviors. The decrease of locomotive behavior has been studied as an anxiety  response  caused  by  excessive  heat  shock  in Drosophila(Ostrowski et al., 2018). However, in our study, the same patterns in locomotive activities were indicative as an  anxiety  response  caused  by  bright  light  stimuli  in  early stages  of  life  instead.  This  indicates  that  stress  stimuli  like bright  light  and  heat  shock  will  cause D. melanogaster to experience a decrease of locomotive activity due to anxiety. In previous studies it also can be seen that stresses such as electric  shock  (Ries  et  al.,  2017)  and  induction  of  anxiety through continuous exposure to vibrating stress stimuli has caused a change in their locomotor behavior (Batsching et al., 2016).

For  the  79598  optogenetic  Chrimson  flies,  there  was  no significant  difference  between  the  control  and  the  stress group in the locomotive assay. This insignificance can arise from the fact that ambient white light could also serve as a stress stimulus for them because the ambient light contains red wavelengths of light, which could activate the Chrimson opsin expressed in pain neurons of the optogenetic flies. This pre-exposure to indirect red light may have caused the pain neurons   to   be   activated   even   before   they   were experimentally  exposed  to  red  light.  As  a  result,  the optogenetics flies did not serve as a model strain for testing the induction of anxiety by activating pain neurons through the usage of red light.

Even  though  WAFO  behavior  did  not  yield  any statistically significant results, a positive trend was observed in the WAFO assay. Where the control groups for both of the strains had lower  percentage  of  WAFO  compared  to  the  stress  groups which showed greater WAFO activities. The insignificance in the data could arise from the low sample size, n = 4. However, due to great variance in the tracking of the video and the low sample size no conclusions can be made. It is because both the graphs in Figure 3C & Figure 4C show non-overlapping error  bars  but  have  insignificant  p-values  (p  >  0.05).  Although,the p-values were not significant, a power analysis showed  that  n=9  of  the  optogenetic  organisms  would  be sufficient enough to obtain significance in our WAFO data at power level of 0.80.

D. melanogaster has been a model organism in a variety of experiments due to its genetic similarities with humans. For this  reason,  alterations  to  the  genes  of  the  organism  may result  in  a  change  in  behavioral  response (Sørensen  et  al., 2005). Thus, this experiment assumed that the larval stage in D. melanogaster was analogous to infancy in humans. After confirming that administering stress to fruit flies at a larval stage influences the organism as an adult. It can be noted that exposing humans to stress during infancy, will play a role in their  behavior  as  adults.  As  the  experiment  demonstrated, anxiety-like   behavior   was   indicated   by   decreased locomotion. In humans these anxiety behaviors may translate into social, verbal, or even mental disorders.

This study can be utilized to assess future experiments in the same field of interest. For example, to further understand the locomotive behavior of anxious flies, it is worth looking into how increasing and decreasing the exposure time to stress stimuli can further affect their locomotive response. Another potential option may be to attempt reversing the effects of the amplified  anxiety  in  the  fruit  flies.  Additionally,  an assessment can be made to test if any permanent damage is caused to the organism due to increased levels of stress and the effects of stress on progeny. A study also can also be made on the  effects  on  the  longevity  of  the  organism  due  to  the increased level of anxiety. Finally, epigenetic effects on the progeny  of  the  stressed  group  can  also  be  explored.  It  has already been suggested that social experiences like isolation can alter the epigenetic landscape involved in transcription and neural function (Agrawal et al., 2018). However, here we can explore how anxiety experiences can alter the epigenetic landscape.


The authors would like to acknowledge the support received by Dr. Kwangwon Lee and Dr. Nathan Fried throughout this project. We also would like to thank Ms. Sarah Johnson, who made it possible for us to use the lab space and by providing all lab equipment readily available to us. 



Agrawal, P., Chung, P., Heberlein, U., and Kent, C.F. (2018). Social isolation-induced epigenetic and transcriptional changes in Drosophila dopaminergic neurons. BioRxiv.

Allsop, S.A., Vander Weele, C.M., Wichmann, R., and Tye,    K.M. (2014). Optogenetic insights on the relationship between   anxiety-related   behaviors   and   social deficits. Frontiers in Behavioral Neuroscience 8.

Babenko, O., Kovalchuk, I., and Metz, G.A.S. (2015). Stress-induced   perinatal   and   transgenerational epigenetic programming of brain development and mental   health.   Neuroscience   &   Biobehavioral Reviews 48, 70–91.Batsching,  S.,  Wolf,  R.,  and  Heisenberg,  M.  (2016). Inescapable  Stress  Changes  Walking  Behavior  in Flies -Learned Helplessness Revisited. PLOS ONE 11, e0167066.

Chao, R., Macía-Vázquez, G., Zalama, E., Gómez-García-Bermejo,  J.,  and  Perán,  J.-R.  (2015).  Automated Tracking  of  Drosophila Specimens.  Sensors  15, 19369–19392.

Gibson, W.T., Gonzalez, C.R., Fernandez, C., Ramasamy, L.,  Tabachnik,  T.,  Du,  R.R.,  Felsen,  P.D.,  Maire,  M.R., Perona,  P.,  and  Anderson,  D.J.  (2015).  Behavioral Responses  to  a  Repetitive  Visual  Threat  Stimulus Express  a  Persistent  State  of  Defensive  Arousal  in Drosophila. Current Biology 25, 1401–1415.

Guru, A., Post, R.J., Ho, Y.-Y., and Warden, M.R. (2015). Making Sense of Optogenetics. International Journal of Neuropsychopharmacology 18, pyv079.

Iliadi, K.G. (2009). The Genetic Basis of Emotional Behavior:  Has  the  Time  Come  for  a  Drosophila Model? Journal of Neurogenetics 23, 136–146.

Min, V.A., and Condron, B.G. (2005). An assay of behavioral plasticity in Drosophila larvae. Journal of Neuroscience Methods 145, 63–72.

Mohammad, F., Aryal, S., Ho, J., Stewart, J.C., Norman,  N.A.,  Tan,  T.L.,  Eisaka,  A.,  and  Claridge-Chang,   A.   (2016).   Ancient   Anxiety   Pathways Influence  Drosophila  Defense  Behaviors.  Current Biology 26, 981–986.

Ostrowski, D., Salari, A., Zars, M., and Zars, T. (2018).  A  biphasic  locomotor  response  to  acute unsignaled    high    temperature    exposure    in Drosophila. PLOS ONE 13, e0198702.

Ries, A.-S., Hermanns, T., Poeck, B., and Strauss, R. (2017). Serotonin modulates a depression-like state in Drosophila responsive to lithium treatment. Nature Communications 8, 15738.

Sørensen, J.G., Nielsen, M.M., Kruhøffer, M., Justesen,  J.,  and  Loeschcke,  V.  (2005).  Full  genome gene expression analysis of the heat stress response in   Drosophila   melanogaster.   Cell   Stress   & Chaperones 10, 312.

Stefan, P. (2012) The Fundamentals of Flying: Simple and Inexpensive  Strategies  for  Employing  Drosophila Genetics in Neuroscience Teaching Laboratories. 10.

Weinstock, M. (2017). Prenatal stressors in rodents: Effects on behavior. Neurobiology of Stress 6, 3–13.

Williams, Z.M. (2016). Transgenerational influence of sensorimotor training on offspring behavior and its  neural  basis  in  Drosophila.  Neurobiology  of Learning and Memory 131, 166–175.Zhong,  L.,  Hwang,  R.Y.,  and  Tracey,  W.D.  (2010). Pickpocket  Is  a  DEG/ENaC  Protein  Required  for Mechanical   Nociception   in   Drosophila   Larvae. Current Biology 20, 429–434.

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