Teaching Neuroscience: Reviving Neuroanatomy, Notes on the 2022 Society for Neuroscience Professional Development Workshop on Teaching.

Students often find neuroanatomy a daunting exercise of rote memorization in a dead language. This workshop was designed to enliven the teaching of neuroanatomy. We recast the topic by extending it to the cellular and sub-cellular levels, animating it by learning to build a brain, and infusing the topic with the lively arts. Due to COVID's interference with the usual schedule of Society for Neuroscience (SfN) events, the 2021 Professional Development Workshop on Teaching was held as a webinar on April 12, 2022 with a follow-up question and answer session on June 7. In this workshop, not only were innovative teaching methods presented, but also the very definition of neuroanatomy was pushed to the limits-even reaching into the molecular and subcellular level. The presenters provided means of engaging students that were no cost, low cost, or well within the reach of most academic institutions. Judging by the attendance, this webinar was quite successful in its goals. Our speakers presented exciting and varied approaches to teaching neuroanatomy. Kaitlyn Casimo presented how the vast resources of the Allen Institute could be employed. Marc Nahmani described how open data resources could be utilized in creating a Course-Based Undergraduate Research Experience (CURE) on neural microanatomy. Erika Fanselow presented novel ways to overcome one of students' big hurdles in grasping neuroanatomy: understanding 3-D relationships. Len White described a creative approach in teaching neuroanatomy by incorporating the humanities, particularly art and literature. This article presents synopses of the presentations, which are written by the four presenters. Additionally, prompted by questions from the viewers, we have constructed a table of our favorite resources. A video of the original presentations as well as links to the subsequent Q & A sessions is available at https://neuronline.sfn.org/training/teaching-neuroscience-reviving-neuroanatomy/.

PROJECT DiViNe: DIVERSE VOICES IN NEUROSCIENCE: Profiles of Rita Levi-Montalcini, Ricardo Miledi, Simon LeVay, Erich Jarvis, and Steve Ramirez.

In this paper we share the first five of what we hope will be many profiles of neuroscientists from historically underrepresented or marginalized groups. This initial collection of profiles, meant to stake out the general territory for future offerings, takes as its subjects a fairly broad range of individuals from Nobel laureates to early career scientists and educators. The goal of this project is to facilitate the dissemination of materials neuroscience educators can use to highlight the scientific contributions and personal stories of scientists from historically marginalized groups, and has been developed more extensively in the Editorial that accompanies this collection (Frenzel and Harrington, 2021). We believe that by sharing these stories, and highlighting the diversity of those who have and will continue to contribute to the field of neuroscience, we can help to foster a more inclusive discipline for our undergraduate students. Each of these profiles is a testament to the respect these contributors hold for their subjects. We hope that others might see this new feature as an opportunity to share the admiration they have for those who have impacted them as colleagues, mentors, and role models.

Measuring Sex Differences in the Corpus Callosum by Undergraduates at a Small and a Large Institution.

Neuroscience students often seem more responsive to laboratory exercises that involve human brains. Here we describe a lab that utilizes human brain MRIs to evaluate a long-standing debate over the presence of sex differences in the human brain, specifically the corpus callosum. Students at both Widener and UCLA measured corpus callosum subregions that were already marked-off as described by Witelson (1989) or by Hofer and Frahm (2006). Statistical analyses revealed sex differences using both schemes after correcting for the size of the midsagittal cortex. Widener students, however, uncovered more sex differences than the UCLA students. Lab instruction for UCLA students occurred during the COVID-19 pandemic. So, lab sessions were completely online. In contrast, Widener students had the benefit of in-person lab instruction. Nonetheless, both the data obtained from the images of the corpus callosi as well as measures of pedagogical efficacy were similar between the two institutions, suggesting that distance learning may be a valuable and viable option. Further, when in person learning is not an option, such as during a pandemic, digital databases serve as invaluable resources for online learning. When these databases are utilized in a hypothesis driven research setting, they can serve as the basis for course-based undergraduate research experiences (CUREs), which are known to benefit students-improving retention in science fields.

FraidyRat: A Virtual Module Examining the Neural Circuitry Underlying Fear Conditioning.

FraidyRat is a teaching tool that allows students to investigate the neural basis of fear conditioning and extinction using a virtual rat with a virtual brain. FraidyRat models well-known phenomena at both a behavioral and neural level. Students use virtual versions of tract tracing, systemic and intracerebrally infused drugs, neural recording, and electrical stimulation to understand the neural substrates underlying the observed behavior. This module helps students develop critical thinking skills in order to deduce immediate cause and effect as well as inductive reasoning to grasp the broader scheme. This module utilizes scaffolded instruction and formative assessment to shape the thinking of students as they unfold and discover the neural mechanisms responsible for fear conditioning and extinction in FraidyRat, which largely reflect what is found in real rats. Experience with this three-week module resulted in students showing significant gains in content knowledge as well as a trend toward gains in critical thinking. An attitudinal questionnaire showed that students had an overall positive experience. This module can be replicated at any institution with just a computer. All materials are available at: https://mdcune.psych.ucla.edu/modules/fraidy-rat.

Teaching Computation in Neuroscience: Notes on the 2019 Society for Neuroscience Professional Development Workshop on Teaching.

The 2019 Society for Neuroscience Professional Development Workshop on Teaching reviewed current tools, approaches, and examples for teaching computation in neuroscience. Robert Kass described the statistical foundations that students need to properly analyze data. Pascal Wallisch compared MATLAB and Python as programming languages for teaching students. Adrienne Fairhall discussed computational methods, training opportunities, and curricular considerations. Walt Babiec provided a view from the trenches on practical aspects of teaching computational neuroscience. Mathew Abrams concluded the session with an overview of resources for teaching and learning computational modeling in neuroscience.

Brain Volume Fractions in Mammals in Relation to Behavior in Carnivores, Primates, Ungulates, and Rodents.

The volume fraction (VF) of a given brain region, or the proper mass, ought to reflect the importance of that region in the life of a given species. This study sought to examine the VF of various brain regions across 61 different species of mammals to discern if there were regularities or differences among mammalian orders. We examined the brains of carnivores (n = 17), ungulates (n = 8), rodents (n = 7), primates (n = 11), and other mammals (n = 18) from the online collections at the National Museum of Health and Medicine. We measured and obtained the VF of several brain regions: the striatum, thalamus, neocortex, cerebellum, hippocampus, and piriform area. We refined our analyses by using phylogenetic size correction, yielding the corrected (c)VF. Our groups showed marked differences in gross brain architecture. Primates and carnivores were divergent in some measures, particularly the cVF of the striatum, even though their overall brain size range was roughly the same. Rodents predictably had relatively large cVFs of subcortical structures due to the fact that their neocortical cVF was smaller, particularly when compared to primates. Not so predictably, rodents had the largest cerebellar cVF, and there were marked discrepancies in cerebellar data across groups. Ungulates had a larger piriform area than primates, perhaps due to their olfactory processing abilities. We provide interpretations of our results in the light of the comparative behavioral and neuroanatomical literature.

Using Online Images to Teach Quantitative Skills via Comparative Neuroanatomy: Applying the Directives of Vision and Change.

Vision and Change calls for increasing the quantitative skills of biology majors, which includes neuroscience majors. Accordingly, we have devised a module to give students practice at regression analyses, covariance, and ANOVA. This module consists of a quantitative comparative neuroanatomy lab in which students explore the size of the hippocampus relative to the brain in 62 different mammalian species-from an anteater to a zebu. We utilize a digital image library (with appropriate metadata) allowing students to quantify the size of the hippocampus as well as obtain an index of the size of the brain in these various species. Students then answer the following questions: (1) Do brains scale with body size? (2) Does the hippocampus scale with brain size? (3) If we control for body size, does the hippocampus still scale with brain size? (4) How does the hippocampus change as a proportion of brain size? (5) Is the proportional scaling of the hippocampus different among primates, carnivores, and other mammals? (6) Do the data provide evidence for mosaic or concerted evolution? Measures of the pedagogical efficacy showed clear and significant gains on a PreTest vs PostTest assessment of material related to the module. An open ended qualitative measure revealed students' perception of the purposes of the module, which were consistent with the learning goals. This module utilizes open access digital resources and can be performed at any institution. All the materials or links to online resources can be found at https://mdcune.psych.ucla.edu/modules/cna.

Teaching with Big Data: Report from the 2016 Society for Neuroscience Teaching Workshop.

As part of a series of workshops on teaching neuroscience at the Society for Neuroscience annual meetings, William Grisham and Richard Olivo organized the 2016 workshop on "Teaching Neuroscience with Big Data." This article presents a summary of that workshop. Speakers provided overviews of open datasets that could be used in teaching undergraduate courses. These included resources that already appear in educational settings, including the Allen Brain Atlas (presented by Joshua Brumberg and Terri Gilbert), and the Mouse Brain Library and GeneNetwork (presented by Robert Williams). Other resources, such as NeuroData (presented by William R. Gray Roncal), and OpenFMRI, NeuroVault, and Neurosynth (presented by Russell Poldrack) have not been broadly utilized by the neuroscience education community but offer obvious potential. Finally, William Grisham discussed the iNeuro Project, an NSF-sponsored effort to develop the necessary curriculum for preparing students to handle Big Data. Linda Lanyon further elaborated on the current state and challenges in educating students to deal with Big Data and described some training resources provided by the International Neuroinformatics Coordinating Facility. Neuroinformatics is a subfield of neuroscience that deals with data utilizing analytical tools and computational models. The feasibility of offering neuroinformatics programs at primarily undergraduate institutions was also discussed.

Undergraduate Neuroscience Education in the U.S.: Quantitative Comparisons of Programs and Graduates in the Broader Context of Undergraduate Life Sciences Education.

The impact of undergraduate neuroscience programs on the broader landscape of life sciences education has not been described. Using data from the National Center for Education Statistics, we found that the number of undergraduate neuroscience programs in the U.S. continues to grow. Within any given institution, neuroscience programs exist alongside a small number of other life sciences undergraduate programs, suggesting that neuroscience is one of few major options from which students can choose from at many institutions. Neuroscience majors constitute a substantial proportion of all life sciences graduates at many institutions, and in several cases, neuroscience majors were the majority of life sciences graduates. Thus, neuroscience programs contribute substantially to life sciences education, and neuroscience is a highly attractive major among undergraduate students where these programs are available. These data have implications for institutions with existing neuroscience programs as well as for institutions seeking to establish a new program.

Gel Scramble: An E-Tool for Teaching Molecular Neuroscience.

In this completely digital teaching module, students interpret the results of two separate procedures: a restriction endonuclease digestion, and a polymerase chain reaction (PCR). The first consists of matching restriction endonuclease digest protocols with images obtained from stained agarose gels. Students are given the sequence of six plasmid cDNAs, characteristics of the plasmid vector, and the endonuclease digest protocols, which specify the enzyme(s) used. Students calculate the expected lengths of digestion products using this information and free tools available on the web. Students learn how to read gels and then match their predicted fragment lengths to the digital images obtained from the gel electrophoresis of the cDNA digest. In the PCR experiment, students are given six cDNA sequences and six sets of primers. By querying NCBI BLAST, students can match the PCR fragments to the lengths of the predicted in silico PCR products. The ruse posed to students is that the gels were inadvertently mislabeled during processing. Although students know the experimental details, they do not know which gel goes with a given restriction endonuclease digest or PCR-they must deduce the answers. Because the gel images are from actual students' experiments, the data sometimes result from mishandling/mislabeling or faulty protocol execution. The most challenging part of the exercise is to explain these errors. This latter aspect requires students to use critical thinking skills to explain aberrant outcomes. This entire exercise is available in a digital format and downloadable for free at http://mdcune.psych.ucla.edu/modules/gel.

ERIN: A Portal to Resources for Higher Education in Neuroscience.

ERIN, Educational Resources in Neuroscience, is the Society for Neuroscience's web portal to selected, high-quality materials for higher education. A Board of Editors approves resources after describing them and classifying them by topic, subtopic, media type, author, and appropriate educational level. Some resources are also accompanied by reviews and ratings from faculty who have used the resource. These features make a search of ERIN far more useful than a typical Google search. ERIN's development was funded by the National Science Foundation with a three-year grant to SfN. Along the way, various unexpected problems arose and solutions were found, many of which are described in this overview of ERIN's history and the various decisions that were made in its design and development.

An Instructor's Guide to (Some of) the Most Amazing Papers in Neuroscience.

Although textbooks are still assigned in many undergraduate science courses, it is now not uncommon, even in some of the earliest courses in the curriculum, to supplement texts with primary source readings from the scientific literature. Not only does reading these articles help students develop an understanding of specific course content, it also helps foster an ability to engage with the discipline the way its practitioners do. One challenge with this approach, however, is that it can be difficult for instructors to select appropriate readings on topics outside of their areas of expertise as would be required in a survey course, for example. Here we present a subset of the papers that were offered in response to a request for the "most amazing papers in neuroscience" that appeared on the listserv of the Faculty for Undergraduate Neuroscience (FUN). Each contributor was subsequently asked to describe briefly the content of their recommended papers, their pedagogical value, and the audiences for which these papers are best suited. Our goal is to provide readers with sufficient information to decide whether such articles might be useful in their own classes. It is not our intention that any article within this collection will provide the final word on an area of investigation, nor that this collection will provide the final word for the discipline as a whole. Rather, this article is a collection of papers that have proven themselves valuable in the hands of these particular educators. Indeed, it is our hope that this collection represents the inaugural offering of what will become a regular feature in this journal, so that we can continue to benefit from the diverse expertise of the FUN community.

A "Four Core Genotypes" rat model to distinguish mechanisms underlying sex-biased phenotypes and diseases.

Background: We have generated a rat model similar to the Four Core Genotypes mouse model, allowing comparison of XX and XY rats with the same type of gonad. The model detects novel sex chromosome effects (XX vs. XY) that contribute to sex differences in any rat phenotype. Methods: XY rats were produced with an autosomal transgene of Sry , the testis-determining factor gene, which were fathers of XX and XY progeny with testes. In other rats, CRISPR-Cas9 technology was used to remove Y chromosome factors that initiate testis differentiation, producing fertile XY gonadal females that have XX and XY progeny with ovaries. These groups can be compared to detect sex differences caused by sex chromosome complement (XX vs. XY) and/or by gonadal hormones (rats with testes vs. ovaries). Results: We have measured numerous phenotypes to characterize this model, including gonadal histology, breeding performance, anogenital distance, levels of reproductive hormones, body and organ weights, and central nervous system sexual dimorphisms. Serum testosterone levels were comparable in adult XX and XY gonadal males. Numerous phenotypes previously found to be sexually differentiated by the action of gonadal hormones were found to be similar in XX and XY rats with the same type of gonad, suggesting that XX and XY rats with the same type of gonad have comparable levels of gonadal hormones at various stages of development. Conclusion: The results establish a powerful new model to discriminate sex chromosome and gonadal hormone effects that cause sexual differences in rat physiology and disease.

Teaching neuroinformatics with an emphasis on quantitative locus analysis.

Although powerful bioinformatics tools are available for free on the web and are used by neuroscience professionals on a daily basis, neuroscience students are largely ignorant of them. This Neuroinformatics module weaves together several bioinformatics tools to make a comprehensive unit. This unit encompasses quantifying a phenotype through a Quantitative Trait Locus (QTL) analysis, which links phenotype to loci on chromosomes that likely had an impact on the phenotype. Students then are able to sift through a list of genes in the region(s) of the chromosome identified by the QTL analysis and find a candidate gene that has relatively high expression in the brain region of interest. Once such a candidate gene is identified, students can find out more information about the gene, including the cells/layers in which it is expressed, the sequence of the gene, and an article about the gene. All of the resources employed are available at no cost via the internet. Didactic elements of this instructional module include genetics, neuroanatomy, Quantitative Trait Locus analysis, molecular techniques in neuroscience, and statistics-including multiple regression, ANOVA, and a bootstrap technique. This module was presented at the Faculty for Undergraduate Neuroscience (FUN) 2011 Workshop at Pomona College and can be accessed at http://mdcune.psych.ucla.edu/modules/bioinformatics.

X chromosome number causes sex differences in gene expression in adult mouse striatum.

Previous research suggests that sex differences in the nigrostriatal system are created by direct effects of the sex chromosomes (XX vs. XY), independent of the action of gonadal hormones. Here we tested for sex chromosome effects on expression of three mRNAs in the striatum and nucleus accumbens of adult mice of the four core genotypes model (XX and XY gonadal males, XX and XY gonadal females). Mice were gonadectomized (GDX) at 47-51 days old to eliminate group differences in the levels of gonadal steroids. Three weeks later, mice were killed and brains collected for in situ hybridization of the striatum, or the striatum was dissected out for quantitative reverse transcriptase-polymerase chain reaction (RT-PCR). Expression in XX and XY mice was measured by in situ hybridization using riboprobes encoding the dynorphin precursor Pdyn (prodynorphin), the substance P precursor Tac1 (preprotachykinin) or dopamine D2 receptor. XX mice had higher expression, relative to XY mice of the same gonadal sex, of Pdyn and Tac1 mRNA in specific striatal regions. Quantitative PCR confirmed that GDX XX mice have higher Pdyn expression in striatum than XY mice, regardless of their gonadal sex. XX had higher Pdyn expression than XY or XO mice, indicating that the sex chromosome effect is the result of XX vs. XY differences in the number of X chromosomes, probably because of sex differences in the expression of X gene(s) that escape inactivation. We detected no sex chromosome effect on D2 receptor mRNA.

Modular Digital Course in Undergraduate Neuroscience Education (MDCUNE): A Website Offering Free Digital Tools for Neuroscience Educators.

We are providing free digital resources for teaching neuroscience labs at http://mdcune.psych.ucla.edu/. These resources will ultimately include materials for teaching laboratories in electrophysiology of neuronal circuits (SWIMMY), a Neuroinformatics/Bioinformatics module, and two modules for investigating the effects of hormones on early CNS development-one focusing on the development of the song system and one focusing on sex differences in spinal cord motor neurons. All of these modules are inquiry based-students gain from genuine experiences in doing actual studies rather than just simulations. These materials should provide instructors the ability to provide good quality laboratory experiences regardless of resource limitations. Currently, modules on sex differences in the spinal cord and virtual neural circuits (SWIMMY) are available on our website. More will be available in summer 2009 and 2010. SWIMMY was demonstrated at the Faculty for Undergraduate Neuroscience (FUN) Workshop-The Undergraduate Neuroscience Education: Interactions, interdisciplines, and curricular best practices at Macalester College in July 2008.

The journal of undergraduate neuroscience education: history, challenges, and future developments.

The 'JUNE and You' sessions presented at the July 2008 Undergraduate Neuroscience Education workshop, sponsored jointly by Faculty for Undergraduate Neuroscience (FUN) and Project Kaleidoscope (PKAL), featured background information about the history and mission of the Journal of Undergraduate Neuroscience Education (JUNE), followed by an informative discussion about the challenges facing JUNE, including new ideas for future developments. This article will highlight some of the information and ideas generated and shared at this conference. Critical discussion points included the need to keep members of FUN actively engaged in submitting and reviewing articles for JUNE. Ways in which authors, reviewers, and interested faculty members could best help in promoting the mission and vision of JUNE were discussed. Concerns about recent hackings into the JUNE website were also raised, and possible solutions and measures that can be taken to minimize this in the future were discussed. In addition, ideas for expanding the role of JUNE to provide a forum to evaluate new and emerging website information that is pertinent to undergraduate neuroscience education was discussed. Ideas for future developments of JUNE included revolving postings of articles as they are accepted, providing links to several related websites, and allowing updates for articles that have been previously published in JUNE. Finally, ideas for maintaining and expanding JUNE's stature as the resource for undergraduate neuroscience education included ensuring that JUNE is listed on important search vehicles, such as PubMed.

A dose-response study of estradiol's effects on the developing zebra finch song system.

To gauge the sensitivity of the female zebra finch song system to estradiol (E2), we used subcutaneous implants to administer various doses of E2 to hatchling female zebra finches. Four different doses of E2 were administered: 50, 15, 5 and 0-microg via subcutaneous silicon "ropes" at hatching, and the brains were examined in adulthood. Further, we examined whether masculinization was all-or-none once a threshold was reached or if the morphology of the song system would show a graded response to the various doses of E2. Finally, we asked if the various dependent measures - volume of song nuclei, neuron size, and neuron number - would show differential sensitivity to E2. Fifteen micrograms was sufficient to masculinize many aspects of the song system and was often as effective as 50-microg, causing a dramatic difference relative to the 0-microg group. Different aspects of the song system seemed differentially sensitive to the effects of E2: volumes of song control nuclei, the size of RA neurons, and the number of HVC neurons were significantly masculinized by 15-microg E2, but the number of RA neurons and HVC and lMAN soma sizes required 50-microg. The results suggest that several developmental processes are influenced by E2, possibly because of multiple sites of action or multiple processes that respond to E2.

SWIMMY: Free Software for Teaching Neurophysiology of Neuronal Circuits.

To circumvent the many problems in teaching neurophysiology as a "wet lab," we developed SWIMMY, a virtual fish that swims by moving its virtual tail by means of a virtual neural circuit. SWIMMY diminishes the need for expensive equipment, troubleshooting, and manual skills that require practice. Also, SWIMMY effectively replaces live preparations, which some students find objectionable. Using SWIMMY, students (1) review the basics of neurophysiology, (2) identify the neurons in the circuit, (3) ascertain the neurons' synaptic interconnections, (4) discover which cells generate the motor pattern of swimming, (5) discover how the rhythm is generated, and finally (6) use an animation that corresponds to the activity of the motoneurons to discover the behavioral effects produced by various lesions and explain them in terms of their neural underpinnings. SWIMMY is a genuine inquiry-based exercise producing data that requires individual thought and interpretation. It is neither a cookbook exercise nor a demonstration. We have used SWIMMY for several terms with great success. SWIMMY solidifies students' understanding of material learned in traditional lecture courses because they must apply the concepts. Student ratings of SWIMMY have been very positive, particularly ratings from students who have also been exposed to a "wet" neurophysiology lab. Because SWIMMY requires only computers for implementation and makes minimal demands on instructional resources, it provides for a great deal of flexibility. Instructors could use SWIMMY as part of a traditional lab course, as a classroom exercise, in distance learning, or in blended instructional formats (internet with classroom). SWIMMY is now available for free online complete with student and instructor manuals at http://mdcune.psych.ucla.edu.

Effects of long-term flutamide treatment during development in zebra finches.

The molecular mechanisms responsible for the sexual differentiation of the zebra finch song system remain mysterious. Androgen receptors are expressed in a sexually dimorphic fashion in the zebra finch song system: males have more cells expressing androgen receptors, and this sex difference appears very early in development (day 9 posthatch). Estrogen administration to hatchling females up-regulates androgen receptor expression in their song system and profoundly masculinizes their song system's morphology. Co-administering flutamide, an androgen receptor blocker, with estrogen impedes estrogen's masculinizing effects on the song system, suggesting that androgens are required for masculine development. Accordingly, to investigate further the role of androgens in the sexual differentiation of the zebra finch song system, we sought to block androgen activity in males by administering large, sustained doses of flutamide from just before androgen receptors are expressed in the song system (day 7) through to the day of sacrifice (days 61-63). Flutamide profoundly reduced the size of the testes, demonstrating that this drug and mode of administration could have a large impact on tissues. In contrast, flutamide had only a minor impact on the song system: the number of RA neurons was slightly reduced, and the corrected HVC volume showed a trend toward demasculinization. Other brain measures (uncorrected HVC, and corrected and uncorrected volumes of Area X, lMAN, RA, and Rotundus; neuron size in lMAN, HVC, and RA; and number of HVC and LMAN neurons) were not significantly affected. The present results do not support an important role for androgen in masculinizing the song circuit after posthatch day 7.