Tools and resources for neuroanatomy education: a systematic review

RESEARCH ARTICLE Open Access Tools and resources for neuroanatomy education: a systematic review M. Arantes 1,2* , J. Arantes 3 and M. A. Ferreira 4 Abstract Background: The aim of this review was to identify studies exploring neuroanatomy teaching tools and their impact in learning, as a basis towards the implementation of a neuroanatomy program in the context of a curricular reform in medical education. Methods: Computer-assisted searches were conducted through March 2017 in the PubMed, Web of Science, Medline, Current Contents Connect, KCI and Scielo Citation Index databases. Four sets of keywords were used, combining “neuroanatomy”with “education”,“teaching”,“learning”and “student*”. Studies were reviewed independently by two readers, and data collected were confirmed by a third reader. Results: Of the 214 studies identified, 29 studies reported data on the impact of using specific neuroanatomy teaching tools. Most of them (83%) were published in the last 8 years and were conducted in the United States of America (65.52%). Regarding the participants, medical students were the most studied sample (37.93%) and the majority of the studies (65.52%) had less than 100 participants. Approximately half of the studies included in this review used digital teaching tools (e.g., 3D computer neuroanatomy models), whereas the remaining used non-digital learning tools (e.g., 3D physical models). Conclusions: Our work highlight the progressive interest in the study of neuroanatomy teaching tools over the last years, as evidenced from the number of publications and highlight the need to consider new tools, coping with technological development in medical education. Keywords: Neuroanatomy, Education, Teaching, Learning, Student Background Among the basic sciences providing relevant medical awareness, human anatomy, which includes gross and neuroanatomy, has historically been considered a key science educational area in medical education [1,2]. The first descriptions of human anatomy teaching in Europe dates back to Greece, in third century BC, with the introduction of systemic human cadaveric dissection. Although the practice of human dissection was prohibited during the Middle Ages due to religious and popular beliefs, it revival at the beginning of fourteenth century and becomes the core basis in medical education and anatomy teaching until the twentieth century [3,4]. By that time, significant changes have occurred in undergraduate medical education, on one hand because of the introduction of new subjects into curricular programmes as medical scientific knowledge increases and on the other hand because of the move towards skillsbased teaching to face clinical practice [5–8]. Within this new reality, many preclinical medical curricula started to integrate systems-based units, abandoning the traditional, isolated, discipline-based curricular approaches [9–14]. These changing concepts greatly influenced the modern teaching of medical anatomy, with many schools now delivering anatomy using integrated, clinicallyoriented modules, with considerably less time allocated to anatomy [15–17]. For example, within the USA contact hours for gross anatomy has fallen from an average of 170 h in 2002 to ~ 150 h in 2012 and in neuroanatomy contact hours decreased from 95 to 83 h from 2002 * Correspondence: [email protected] 1 Department of Biomedicine, Unit of Anatomy, Faculty of Medicine of the University of Porto, Al. Prof. Hernâni Monteiro, 4200 –319, Porto, Portugal 2 Division of Neuroradiology, Department of Radiology, Portuguese Institute of Oncology, Porto, Portugal Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Arantes et al. BMC Medical Education (2018) 18:94 https://doi.org/10.1186/s12909-018-1210-6 to 2012 [18]. This general reduction in time dedicated to anatomy teaching at medical schools, associated with the increased demand for clinical importance of the topics covered in anatomy curricula, have led to a redefinition of program content and students’learning objectives, accompanied by the introduction of innovative teaching and learning approaches. Despite the long history, the role of cadaveric dissection, as the primary tool for anatomical teaching, has been reduced or replaced in most medical schools by prosection, use of plastic models and/or multimedia-based learning packages [19]. Although initially integrated with the teaching of gross anatomy, neuroanatomy can now be found as a stand-alone course or, most frequently, as an integrated part of the systems-based approach, taught alongside other neurosciences. Teaching of neuroanatomy to students is known to be particularly challenging, due to the sheer complexity and interconnectedness of the central nervous system [20]. Students are required to learn not only anatomical structures, but also be able to understand their topography, spatial relationships and clinical significance. In 1994, Jozefowicz [21] introduced the term “neurophobia”as “a fear of the neural sciences and clinical neurology that is due to the students’inability to apply their knowledge of basic sciences to clinical situations”. In fact, poor teaching and the challenging nature of aspects of neuroanatomy were identified, in one study, as reasons for considering neurosciences/ neurology so difficult. To face changes in medical education curricula and to help reduce neurophobia, some anatomists have developed and implemented innovative teaching techniques and strategies. In this context, Moxham et al. [22]alsoproposedacore syllabus for teaching neuroanatomy to medical students, to provide guidelines concerning neuroanatomical knowledge. However, the debate over how best to teach neuroanatomy in undergraduate medical education continues, with each institution using its own method. The major aim of the present work is to review the most common methods for teaching neuroanatomy, and their effectiveness. More specifically, we intend to: a) identify the studies that explore neuroanatomy teaching tools; and b) to assess their impact on learning. Methods Databases searched and search terms The electronic databases searched in this review included those identified as the most relevant to the topic. More specifically, computer-assisted searches were conducted in six online databases: PubMed, Web of Science, Medline, Current Contents Connect, KCI and Scielo Citation Index. As keywords, four sets were used, combining “neuroanatomy”with “education”,“teaching”,“learning”and “student*”. Inclusion and exclusion criteria The search was restricted to English-language studies that focus on the teaching of neuroanatomy. A comprehensive search was performed for papers available for search from each database’s inception through March 2017. Papers available online ahead of the print version were also analyzed. Manuscripts were included if they were original research studies assessing the impact of using a specific method on student’s learning of neuroanatomy. The exclusion criteria were as follows: i) descriptive studies on the use of a teaching method without assessing the impact on learning; ii) studies describing the development of a teaching method; iii) studies not focused on the teaching of human neuroanatomy; iv) studies in languages other than English; v) reviews, editorial material, proceeding papers, notes, letters to the Editors and meeting abstracts; and vi) duplicate papers. Selection of papers All databased were reviewed independently by two readers (M.A. and J.A.) using the above stated criteria. More specifically, each manuscript identified was placed on an Excel spreadsheet, and the readers applied the exclusion criteria independently. Disagreements were discussed in a meeting and resolved by consensus. After removal of duplicate manuscripts, all potentially eligible manuscripts were screened by both readers. Then, the full text of all screened manuscripts was carefully read. All data collected was confirmed by a third reader (M.F.), and discussions occurred until a final consensus was reached. Charting collating and summarizing the data Spreadsheets were used to register the most important features of each study, namely the title of the papers, authors, year of publication, university and country where the study was conducted, type and number of participants, teaching tool, aim, methodology, number of participants, and main results/conclusions. Data were summarized, and were then grouped according to these features. Results Studies included in this review The search of PubMed, Web of Science, Medline, Current Contents Connect, KCI and Scielo Citation Index databased yielded 214 manuscripts. After removal of duplicate studies (n= 92), a total of 122 manuscripts were identified. On applying the inclusion and exclusion criteria by the two independent readers, 53 manuscripts were excluded because they were written in languages other than English, were abstracts, letters to the Editors, editorial material, proceeding papers, or notes. Therefore, a total of 69 manuscripts were then assessed for eligibility. After these manuscripts were read in their Arantes et al. BMC Medical Education (2018) 18:94 Page 2 of 15 entirety, 40 studies were excluded because they were descriptive reports of a teaching method without assessing its effectiveness, they described the development of a new teaching tool, did not focused on the learning of neuroanatomy (e.g., neuroanatomy of schizophrenic patients) or were review manuscripts. Thus, a total of 29 manuscripts meet the criteria to be included in this review (see Fig. 1). Table 1presents some of the features of the papers included in the present work. Of the 29 studies, the first study [36] was published 50 years ago, in 1966. However, the majority of the studies (n= 15; 52%) were published in 2012–2016, and 24 (83%) of the studies found were published in the last 8 years. Only 4 (14%) were published before 2005. Most studies were conducted in the United States of America (n= 19; 65.52%), followed by the United Kingdom (n= 4; 13.79%) and Australia (n=2; 6.90%). The remaining four studies were from Canada, India, Poland and Spain. Regarding the type of participants, medical students are the most studied sample (n= 11; 37.93%), followed by psychology students (n= 4; 13.79%), non-specified undergraduate students with neuroanatomy experience (n= 4; 13.79%), biology students (n= 3; 10.34%), psysical/occupational therapy students (n= 3; 10.34%), and volunteers without neuroanatomy experience (n= 3; 10. 34%). Only one study (3.45%) investigated the effect of a neuroanatomy teaching tool on faculty members. Although 10 studies (34.48%) had 100 or more participants, the remaining 19 (65.52%) had a number of participants less than 100. One study only presented 13 students as participants. The teaching methods used in the studies included in this review can be classified into digital tools (n= 13; 46. 43%) and non-digital learning tools (n= 15; 53.57%). The digital tools include 3D computer neuroanatomy models, computer-based tools (i.e., computer-aided instruction/ learning), and apps installed in tablets. The non-digital tools include the use of case studies, equivalence-based instruction (EBI), 3D physical models, face-to-face teaching, flipped classroom, inquiry-based laboratory instruction, intensive mode of delivery, interpolation of questions, near-peer teaching, Renaissance artists’depictions, selfinstructional stations, and truncated lectures, conceptual exercises and manipulatives. Digital tools Computer-based neuroanatomy tools Table 2summarizes each study included in this review, including the teaching tool used, aims, methodology employed, and main results/conclusion. Some researchers [23–28] focused their studies on the impact of using computer-based tools for teaching neuroanatomy. More specifically, McKeough et al. [23,24] investigated the effect of a computer-based tool on students’performance and their attitudes. Before and after test questions revealed that scores improved significantly after working with the learning model. In addition, students reported the computer-aided neuroanatomy learning modules as a valuable and enjoyable learning tool, and perceived their clinical-self efficacy as higher as a result of working with them. Foreman et al. [25] conducted a prospective evaluation by asking questions to the students regarding tool Fig. 1 Process applied to identify the manuscripts Arantes et al. BMC Medical Education (2018) 18:94 Page 3 of 15 Table 1 Main features of the manuscripts included in this review (n= 29) Features Number (%) Studies Publication year 2012–2016 15 (51.72) I, II, III, IV, V, VI, VII, VIII, IX, X, XI, XII, XIII, XIV, XV 2007–2011 9 (31.03) XVI, XVII, XVIII, XIX, XX, XXI, XXII, XXIII, XXIV 2002–2007 1 (3.45) XXV 1966–2001 4 (13.79) XXVI, XXVII, XXVIII, XXIX Place of the study Australia Canada India Poland Spain UK USA 2 (6.90) 1 (3.45) 1 (3.45) 1 (3.45) 1 (3.45) 4 (13.79) 19 (65.52) XI, XIII I V XVIII VIII II, III, XII, XXIII IV, VI, VII, IX, X, XIV, XV, XVI, XVII, XIX, XX, XXI, XXII, XXIV, XXV, XXVI, XXVII, XXVIII, XXIX Type of participants Faculty members and students 1 (3.45) XXII Master’s degree health care professional students 1 (3.45) XXI Non-specified undergraduate students with neuroanatomy experience 4 (13.79) VI, VIII, XI, XIII Participants without neuroanatomy experience 3 (10.34) VII, IX, XVI Undergraduate or graduate biology students 3 (10.34) XIV, XVII, XXIV Undergraduate biomedical students 1 (3.45) II Undergraduate medical students 11 (37.93) I, III, IV, V, XII, XVIII, XX, XXIII, XXVII, XXVIII, XXIX Undergraduate psychology students 4 (13.79) X, XIV, XV, XXVI Undergraduate or graduate physical/ocupational therapy students 3 (10.35) XIX, XXIV, XXV Number of participants + 201 3 (10.35) II, XVIII, XXIII 151–200 3 (10.35) XIII, XXVII, XXVIII 101–150 4 (13.79) V, XI, XX, XXIX 51–100 11 (37.93) IV, VI, VII, VIII, IX, XII, XV, XVI, XIX, XXI, XXII, 0–50 8 (27.59) I, III, X, XIV, XVII, XXIV, XXV, XXVI Teaching tool Digital tool 14 (50.00) I, II, IV, VII, VIII, IX, XVI, XIX, XX, XXI, XXII, XXIII, XXV, XXVII Non-digital tool 14 (50.00) III, V, VI, X, XI, XII, XIII, XIV, XV, XVII, XXIV, XXVI, XXVIII, XXIX Type of teaching tool 3D computer neuroanatomy tools 3D physical models Apps installed in tablets Case studies Computer-based neuroanatomy tools Equivalence-based instruction, EBI Face-to-face teaching Flipped classroom Inquiry-based laboratory instruction Intensive mode of delivery Interpolation of questions Near-peer teaching Renaissance artists’depictions Self-instructional stations Truncated lectures, conceptual exercises and manipulatives 6 (21.43) 1 (3.57) 1 (3.57) 3 (10.71) 6 (21.43) 2 (7.14) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) 1 (3.57) I, IV, VII, VIII, IX, XVI, XX II XIV XIX, XXI, XXII, XXIII, XXV, XXVII III, XV XIII V VI XI XXIX XII X XXVIII XXIV Arantes et al. BMC Medical Education (2018) 18:94 Page 4 of 15 Table 2 Summary description of the 29 studies included in this review (listed by year of publication) Title Authors (year) University, country Participants (number) Teaching tool Aim Methodology Main results/conclusion Evaluation of an online three-dimensional interactive resource for undergraduate neuroanatomy education I Allen et al. (2016) Western University, Canada Second-year undergraduate medical students (n= 47) 3D computer neuroanatomy model (digital tool) To evaluate the impact on learning of a novel, interactive 3D neuroanatomy model. Participants were divided into 2 groups, each accessing 2 learning modalities (3D model and a cadaveric laboratory session). After each modality, students completed a test. (mix betweenand withinsubject design) Participants were pleased to work with the 3D model. In addition, their learning outcomes significantly improved after accessing this teaching tool. Mobile technology: students perceived benefits of apps for learning neuroanatomy II Morris et al. (2016) University of Leeds, UK Undergraduate biomedical students enrolled in a level 2 course (n=519) 5 apps installed in tablet (Apple iPad) devices (digital tool) To examine the students’use of apps in a neuroanatomy practical class: their perceptions and learning outcomes. There were three cohorts of students (3-year study). The neuroanatomy practical session included the use of tablet devices. After the session the students completed a questionnaire about the use of the apps. Students made extensive use of the apps, considered them easy to use and beneficial for learning. Compared with the year before the trial started, there was an increase in the students’performance. The student experience of applied equivalence-based instruction for neuroanat omy teaching III Greville et al. (2016) Swansea University, UK Firstand secondyear undergraduate medical students (n= 43) Equivalence-based instruction, EBI (non-digital tool) To develop and assess the effectiveness of EBI learning resources. Initially participants completed a pre-test. Then the learning of the relations occurred, followed by a post-test design to assess students’learning. (withinsubject design) The EBI resources were an effective, efficient and wellreceived method for teaching neuroanatomy. Development and assessment of a new 3D neuroanatomy teaching tool for MRI training IV Drapkin et al. (2015) Brown University, USA First-year undergraduate medical students (n= 73) 3D computer neuroanatomy model (digital tool) To create and evaluate the efficacy of a computerized 3D neuroanatomy teaching tool Participants were divided into two groups. The first group was taught using the 3D teaching tool, and the second using traditional methods. Scores from an MRI identification quiz and survey were compared. (between-subject design) The 3D teaching tool was an effective way to train students to read an MRI of the brain and particularly effective for teaching Cshaped internal brain structures. Perception of MBBS students to “flipped class room”approach in neuroanatomy module V Veeramani et al. (2015) Jawaharlal Institute of Postgraduate Medical Education and Research, India First-year undergraduate medical students (n= 130) Flipped classroom (non-digital tool) To examine the impact of a flipped classroom approach (i.e., assess students’ perception and the impact on their performance and attitudes) Preand post-tests were designed to test the learning aims of the session. The perception of the students was also assessed. (withinsubject design) Results showed significant differences between the pre and post-test scores. Student response to the flipped classroom structure was largely positive A mind of their own: Using inquiry-based teaching to build critical thinking skills and intellectual engagement in an under Greenwald & Quitadamo (2014) A regional university in the Pacific Northwest, USA Undergraduate students enrolled in a human neuroanatomy course (n=85) Inquiry-based clinical case, IBCC (nondigital tool) To determine which teaching method (conventional and IBCC) produces greater gains in Participants were divided into two groups: conventional and Experimental group. All students were analyzed for Using the California critical thinking skills test, students in the conventional neuroanatomy course gained less than 3 national Arantes et al. BMC Medical Education (2018) 18:94 Page 5 of 15 Table 2 Summary description of the 29 studies included in this review (listed by year of publication) (Continued) Title Authors (year) University, country Participants (number) Teaching tool Aim Methodology Main results/conclusion graduate neuroanatomy course VI critical thinking and content knowledge exam and course grade performance. Critical thinking preand posttests were analyzed. (mix betweenand withinsubject design) percentile ranks, whereas IBCC students gained over 7.5 within one academic term. Computer-based learning: graphical integration of whole and sectional neuroanatomy improves long-term retention VII Naaz et al. (2014) University of Louisville, USA Volunteers between 16 and 34 years, with minimal or no knowledge of neuroanatomy (n= 64) 3D computer neuroanatomy models (digital tool) To examine if instruction with graphically integrated representations of whole and sectional neuroanatomy is effective Participants were divided into two groups. After a pretest, participants learned sectional anatomy using one of the two learning programs: sections only or 2-D/3-D. Then tests of generalization were completed. (betweensubject design) It showed that the use of graphical representation helps students to achieve a deeper understanding of complex spatial relations Enhancing neuroanatomy education using computer-based instructional material VIII Palomera et al. (2014) University of Salamanca, Spain Undergraduate students enrolled in a medical anatomy course (n=65) 3D computer neuroanatomy models (digital tool) To develop a computer-based tool based on 3D images, and to examine if the for this tool depends on their visuospatial ability Participants completed an online rating-scale to measure the educational value that they assigned to the teaching tool. In addition, the student’s visuospatial aptitude was assessed. (between-subject design) Findings showed that students assigned a high educational value to this tool, regardless of their visuospatial skills. Computer-based learning: Interleaving whole and sectional representation of neuroanatomy IX Pani et al. (2013) University of Louisville, USA Undergraduate students with rudimentary knowledge of neuroanatomy (n= 59) 3D computer neuroanatomy model (digital tool) To compare a basic transfer method for learning whole and sectional neuroanatomy with a method in which both forms of representation were interleaved. There were 3 experimental conditions: i) section only, ii) whole then sections; and iii) alternation. (betweensubject design) Interleaved learning of whole and sectional neuroanatomy was more efficient than the basic transfer method. Da Vinci coding? Using renaissance artists’ depictions of the brain to engage student interest in neuroanatomy X Watson (2013) Lewis & Clark College, USA Undergraduate psychology students (n= 27) Renaissance artists’ depictions of the central nervous system (non-digital tool) To increase students’ interest in the study of neuroanatomy There were interactive classroom exercises using well-known Renaissance artists’depictions of the brain. Then participants completed a feedback questionnaire. These exercises increased the interest of the students in the topic. The authors suggest that these exercises may be a useful addition to courses that introduce or review neuroanatomical concepts. Intensive mode delivery of a neuroanatomy unit: Lower final grades but higher student satisfaction XI Whillier, & Lystad, (2013) Macquarie University, Australia Undergraduate students enrolled in the traditional and intensive neuroanatomy units (n= 125) Intensive mode of delivery (non-digital tool) To compare the intensive and traditional units of neuroanatomy for undergraduate students. The intensive mode neuroanatomy unit showed the students the same quantity and quality of material to the same standard, including the Students obtained lower final grades in the new intensive mode delivery but reported having similar overall satisfaction with Arantes et al. BMC Medical Education (2018) 18:94 Page 6 of 15 Table 2 Summary description of the 29 studies included in this review (listed by year of publication) (Continued) Title Authors (year) University, country Participants (number) Teaching tool Aim Methodology Main results/conclusion hours. However, the material was delivered in a shorter timeframe. (between-subject design) their laboratory practical classes. Near-peer teaching in clinical neuroanatomy XII Hall et al. (2013) University of Southampton, UK Undergraduate medical students (n= 60) Near-peer teaching (non-digital tool) To develop and deliver a near-peer programme of study. Two medical students organized and delivered the teaching to their colleges in a series of seven sessions. At the end of each session, participants were asked to fill a feedback questionnaire. (within-subject design) Students’perceived level of knowledge increased after the near-peer teaching sessions, supporting the use of this teaching tool in neuroanatomy courses. The effect of face-to-face teaching on student knowledge and satisfaction in an undergraduate neuroanatomy course XIII Whillier & Lystad, (2013) Macquarie University, Australia Undergraduate students enrolled in the new and old neuroanatomy units (n= 181) Face-to-face teaching (non-digital tool) To examine if faceto-face teaching has an impact on student performance and overall satisfaction with the course. Two groups of students (old and restructured unit of neuroanatomy) were analyzed. A questionnaire was used to compare them in terms of the rate they gave to the course, satisfaction, and final grades. (between-subject design) The increase in total faceto-face teaching hours in the restructured unit of neuroanatomy does not improve student grades. However, it does increase student satisfaction. Using case studies as a semester-long tool to teach neuroanatomy and structure-function relationships to undergraduates XIV Kennedy (2013) Denison Univer, USA Undergraduate biology and psychology students (n= 50) Case studies (nondigital tool) To investigate the effect of teaching neuroanatomy through presentation and discussion of case studies. Students were expected to collaborate with their colleges in small groups. In each case study, the entire class was asked to participate in some aspect of the case. Students report enjoying learning brain structure using this method, and commented positively on the class activities associated with learning brain anatomy. Using equivalence-based instruction to increase efficiency in teaching neuroanatomy XV Pytte & Fienup (2012) Queens College, USA Undergraduate students, primarily of psychology majors (n= 93) Equivalence-Based Instruction, EBI (non-digital tool) To study if EBI is effective in teaching neuroanatomy in a large classroom setting Fourteen brain regions were identified, and conditional relations were explicitly taught during three lectures. Then, students completed test to evaluate some relations that were taught and some not taught. Selection of associations by the teacher can encourage the spontaneous emergence of novel associations within a concept or category. Therefore, it can increase the efficiency of teaching. Computer-based learning of neuroanatomy: a longitudinal study of l learning, transfer, and retention XVI Chariker et al. (2011) University of Louisville, USA Undergraduate students who reported minimal knowledge of neuroanatomy (n= 72) 3D computer neuroanatomy model (digital tool) To determine the effectiveness of new methods for teaching neuroanatomy with computer-based instruction Using a 3D graphical model of the human brain, students learned either sectional anatomy alone (with perceptually continuous or discrete navigation) or whole anatomy followed by sectional anatomy. Results showed efficient learning, good long-term retention, and successful transfer to the interpret ation of biomedical images. They suggest that computer-based learning can be a valuable teaching tool. Arantes et al. BMC Medical Education (2018) 18:94 Page 7 of 15 Table 2 Summary description of the 29 studies included in this review (listed by year of publication) (Continued) Title Authors (year) University, country Participants (number) Teaching tool Aim Methodology Main results/conclusion Participants were tested immediately and after 2–3 weeks. (betweensubject design) Human brains engaged in rat brains: student-driven neuroanatomy research in an introductory biology lab course XVII Gardner et al. (2011) Purdue University, USA First-year undergraduate students interested in majoring in biology (n= 13) Inquiry-based laboratory instruction (non-digital tool) To increase student interest in biology by exposing them to novel research projects Students acquired basic lab skills within the context of a research question of a member of the faculty. Biology students who were not taking the researchbased, Bio-CASPiE course, formed the comparison group for preand postsemester questionnaires. (mix between-withinsubject design) The inquiry-based laboratory instruction increased students’ motivation and excitement, encouraged good scientific practices, and can potentially benefit depart mental research. The study techniques of Asian, American, and European medical students during gross anatomy and neuroanatomy courses in Poland XVIII Zurada et al. (2011) Medical University in Poland, Poland International medical students, from the Polish, American, and Taiwanese divisions (n= 705) –To investigate similarities and differences among American, Asian, and European medical students in terms of their study methods. Participants completed a questionnaire in which they reported which methods they used to study, and which of the methods they believed were most efficient for comprehension, memorization, and review. (between-subject design) Results showed some differences in study techniques among students from the different ethnic backgrounds (e.g., Polish and American preferred the use of dissections and prosected specimens) Effectiveness of a computer-aided neuroanatomy program for entry-level physical therapy students: anatomy and clinical examination of the dorsal column-medial lemniscal system XIX McKeoughet al. (2010) California State University & University of the Pacific, USA Undergraduate physical therapy students (n=61) Computer-aided instruction, CAI (digital tool) To determine if a computeraided instruction learning module improves students’ neuroanatomy knowledge Students completed a paper-and-pencil test on the neuroanatomy/ physiology and clinical examination of the DCML system, both before and after working with the teaching tool (within-subject design) Findings showed that clinical examination posttest scores improved significantly from the pre-test scores A Novel Three-Dimensional Tool for Teaching Human Neuroanatomy XX Estevez et al. (2010) Boston University School of Medicine, USA First-year undergraduate medical students (n= 101) 3D physical neuroanatomy model (digital tool) To develop and assess a new tool forg teaching 3D neuroanatomy to first-year medical students First, all students were presented to traditional 2D methods. Then, the experimental group constructed 3D color-coded physical models, while the control group re-examined 2D brain cross-sections. (between-subject design) 3D computer model was an effective method for teaching spatial relationships of brain anatomy and seems to better prepare students for visualization of 3D neuroanatomy Attitudes of health care students about computerMcKeough& Bagatell (2009) A University in the West Coast, USA Master’s degree health care Computer-aided instruction, CAI (digital tool) To examine students’ attitudes toward CAI, which factors help Three computer-aided neuroanatomy learning modules were used. Stu The CAI modules examined in this study were effective as adjuncts to lecture in Arantes et al. BMC Medical Education (2018) 18:94 Page 8 of 15 Table 2 Summary description of the 29 studies included in this review (listed by year of publication) (Continued) Title Authors (year) University, country Participants (number) Teaching tool Aim Methodology Main results/conclusion aided neuroanatomy instruction XXI professional students (n= 77) their development, and their implications. dents independently reviewed the modules as supplements to lecture and completed a survey to evaluate teaching effectiveness (within-subject design) helping the students learn and make clinical applications of neuroanatomy information A usability study of users’ perceptions toward a multimedia computerassisted learning tool for neuroanatomy XXII Gould et al. (2008) University of Kentucky & University of Louisville & Nova Southeastern University, USA Faculty and students from some institutions across the country (n= 62) Computer-aided instruction, CAI (digital tool) To assess users’ perceptions of the computer-based tool: “Anatomy of the Central Nervous System: A Multimedia Course” First, participants used the multimedia prototype. Then they completed a usability questionnaire designed to measure two usability properties: program need and program applicability This study showed that the CAI was well-designed for all users, and demonstrates the importance of integrating quality properties of usability with principles of human learning. Attitudes to e-learning, learning style and achievement in learning neuroanatomy by medical students XXIII Svirko & Mellanby (2008) Oxford University, UK Second-year preclinical undergraduate medical students (n= 205) Computer-aided learning, CAL (digital tool) To investigate the impact of an online course on encouraging students to learn and their academic performance. The students approach to learning towards the CAL course and towards their studies in general was compared. Student attitudes and ratings were also assessed. Findings revealed that students reported using significantly less deep approach to learning for the CAL course. Using truncated lectures, conceptual exercises, and manipulatives to improve learning in the neuroanatomy classroom XXIV KrontirisLitowitz (2008) Youngstown State University, USA Undergraduate biology and graduate biology and physical therapy students (n= 19) Truncated lectures, conceptual exercises, and manipulatives (non-digital tool) To use truncated lectures, conceptual exercises, and manipulatives to make learning more effective and increase critical thinking The curriculum was revised. More specifically, it became shorter, included practice problems that presented the spinal tracts in an applied context, and included a manipulative. Student’s learning was then assessed and compared with previous classes. (between-subject design). Students’learning was more effective under the revised curriculum, suggesting that this revised curriculum could potentially be applied to other topics. Design and utility of a web-based computerassisted instructional tool for neuroanatomy self-study and review for physical and occupational therapy graduate students XXIV Foreman et al. (2005) University of Utah, USA Undergraduate physical therapy and occupational therapy students (n=43) Computer-assisted instruction, CAI (digital tool) To develop a CAI, and assess their design and utility to teach neuroanatomy. A questionnaire addressed navigation, clarity of the images, benefit of the CAI tool, and students rating. Students were also asked to compare this tool with traditional learning tools. Design and utility of a web-based computerassisted instructional tool for neuroanatomy self-study and review for physical and occupational therapy graduate students XXIV A neuroanatomy teaching activity using case studies and collaboration XXVI Sheldon (2000) University of Michigan, USA Undergraduatestudents of an introductory psychology course (n= 28) Case studies and collaboration (non-digital tool) To evaluate an easier and less time-consuming Students collaborated and applied Findings showed that students assessed this method as very Arantes et al. BMC Medical Education (2018) 18:94 Page 9 of 15