Table 2 Summary description of the 29 studies included in this review (listed by year of publication)

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 between- and within- subject 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 neuroanatomy teaching^III

Greville et al. (2016)

Swansea University, UK

First- and second-year 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. (within-subject design)

The EBI resources were an effective, efficient and well-received 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 C-shaped 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)

Pre- and post-tests were designed to test the learning aims of the session. The perception of the students was also assessed. (within- subject 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 undergraduate neuroanatomy course^VI

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 (non-digital tool)

To determine which teaching method (conventional and IBCC) produces greater gains in critical thinking and content knowledge

Participants were divided into two groups: conventional and Experimental group. All students were analyzed for exam and course grade performance. Critical thinking pre- and post- tests were analyzed. (mix between- and within- subject design)

Using the California critical thinking skills test, students in the conventional neuroanatomy course gained less than 3 national 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. (between- subject 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. (between-subject 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 hours. However, the material was delivered in a shorter timeframe. (between-subject design)

Students obtained lower final grades in the new intensive mode delivery but reported having similar overall satisfaction with 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 face-to-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 face-to-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 (non-digital 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 llearning, 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. Participants were tested immediately and after 2–3 weeks. (between-subject design)

Results showed efficient learning, good long-term retention, and successful transfer to the interpretation of biomedical images. They suggest that computer-based learning can be a valuable teaching tool.

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 research-based, Bio-CASPiE course, formed the comparison group for pre- and post-semester questionnaires. (mix between-within- subject design)

The inquiry-based laboratory instruction increased students’ motivation and excitement, encouraged good scientific practices, and can potentially benefit departmental 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 back- grounds (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 computer- aided 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 post-test 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 computer-aided neuroanatomy instruction^XXI

McKeough& Bagatell (2009)

A University in the West Coast, USA

Master’s degree health care professional students (n = 77)

Computer-aided instruction, CAI (digital tool)

To examine students’ attitudes toward CAI, which factors help their development, and their implications.

Three computer-aided neuroanatomy learning modules were used. Students independently reviewed the modules as supplements to lecture and completed a survey to evaluate teaching effectiveness (within-subject design)

The CAI modules examined in this study were effective as adjuncts to lecture in helping the students learn and make clinical applications of neuroanatomy information

A usability study of users’ perceptions toward a multimedia computer-assisted 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 pre-clinical 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

Krontiris-Litowitz (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 computer-assisted 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 computer-assisted 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 method for teaching neuroanatomy.

Students collaborated and applied their neuroanatomy knowledge to several case studies during classes.

Findings showed that students assessed this method as very enjoyable and helpful for remembering or learning the material.

Computer-based neuroanatomy laboratory for medical students^XXVII

Lamperti & Sodicoff (1997)

Temple University, USA

First-year undergraduate medical students (n = 185)

Computer-based neuroanatomy laboratory (digital tool)

To develop a computer-based laboratory program to substitute the traditional glass-slide laboratory

They compared the performances of those classes that previously had the traditional laboratory with two succeeding classes that used computer program (between-subject design).

Test scores showed that the students’ performance on laboratory material was similar in both classes.

Teaching of neuroanatomy by means of self-instructional laboratory stations^XXVIII

Fisher et al. (1980)

University of Michigan Medical School, USA

First-year undergraduate medical students (n = 200)

Self-instructional stations (non-digital tool)

To teach neuroanatomy using self-instructional laboratory stations

Neuroanatomical laboratory material was presented in a series of six self-instructional stations. Five weeks later, short examinations tests occurred.

Results of the tests indicated a mastery of station material as defined by the objectives and an ability to use the material in applied problems.

Cognitive processes in learning neuroanatomy^XXIX

Geeartsma & Matzke (1966)

University of Kansas, USA

First-year undergraduate medical students (n = 107)

Interpolation of questions (non-digital tool)

To investigate the effect of interpolation of questions into a lecture presentation.

Participants were divided into 2 matched groups. Each group was shown lectures on the visual system which differed only in regard to taxomic level of 10 questions posed lecture. Performance was then measured (between-subject design).

Emphasis on recall questions aids performance on subsequent recall questions more than emphasis on problem-solving questions helps in the solution of subsequent problem-solving questions.