Abstract
Background
Psychology has seen a recent explosion in the use of non-invasive brain stimulation (NIBS) to understand cognition. The prevalence of techniques such as transcranial direct current stimulation (tDCS) in published research has grown immensely in the past decade; however, there has been little effort to incorporate these techniques into the undergraduate curriculum through course-based undergraduate research experiences (CUREs).
Objective
To demonstrate the feasibility of creating a CURE focused on tDCS and to offer practical advice on how to create one at other institutions.
Method
I present a novel undergraduate CURE focused on tDCS, as well as practical advice on how to teach about and safely implement student-driven tDCS experiments.
Results
Undergraduate students learned about and engaged first-hand in their own non-invasive brain stimulation research in an upper-level psychology laboratory course.
Conclusion
An undergraduate laboratory course that focuses on non-invasive brain stimulation has a range of potential benefits for students and instructors alike. Furthermore, it allows undergraduates to gain experience using a rapidly growing neuroscientific methodology.
Teaching Implications
Given that tDCS is a safe and relatively inexpensive method of modulating brain function, the present course demonstrates the ease, and potential advantages, of incorporating NIBS into the undergraduate psychology curriculum.
Keywords
An important goal for undergraduate STEM education is to provide students with research opportunities that will best prepare them to pursue advanced degrees or careers in these fields (Kardash, 2000; Kremer & Bringle, 1990; President’s Council of Advisors on Science and Technology, 2012; Russell et al., 2007; Seymour et al., 2004). In STEM fields, these experiences occur in a variety of formats, including paid and unpaid research opportunities (Hunter et al., 2007; Kardash, 2000; Seymour et al., 2004) as well as course-based undergraduate research experiences (CUREs; Auchincloss et al., 2014; Chase et al., 2020; Mordacq et al., 2017).
There is a significant body of evidence confirming the specific benefits of CUREs in a range of STEM fields including biology (Brownell et al., 2012), chemistry (Williams & Reddish, 2018), and psychology (Dvorak & Hernandez-Ruiz, 2019; Hernandez-Ruiz & Dvorak, 2020; Sathy et al., 2020). For instance, CUREs lead to an increased interest in pursuing graduate school and careers in science (Corwin et al., 2015; Harrison et al., 2011). They result in higher information literacy as well as increased understanding of the processes of science (Lloyd et al., 2019). Such experiences lead to improved communication skills (Seymour et al., 2004) and conceptual understanding (Shaffer et al., 2010; Ward et al., 2014). They also create a fuller sense of project ownership (Hanauer et al., 2012) and a greater interest in laboratory exercises (Brodl, 2005). Finally, the opportunity to engage in course-based research leads to greater diversity and inclusivity in STEM disciplines (Bangera & Brownell, 2014; Barlow & Villarejo, 2004; Jones et al., 2010; Nagda et al., 1998; Rodenbusch et al., 2016; Theobald et al., 2020). There are also documented benefits to faculty who engage in CUREs including strengthening the connection between an instructor’s teaching and research, student projects that result in peer-reviewed publications, and positive evaluation of such teaching opportunities in the tenure and promotion process (Shortlidge et al., 2016).
Course-based undergraduate research experiences have become increasingly common in several branches of neuroscience (Himmel et al., 2020; Thibodeau, 2011); however, fields such as cognitive neuroscience pose unique challenges for undergraduate involvement, especially in course-based research opportunities (Hauk, 2020; Steinmetz & Atapattu, 2010). One of the difficulties relates to the fact that the most common research methodologies in cognitive neuroscience (e.g., functional brain imaging techniques such as fMRI and electrophysiological technique such as EEG) are not only expensive, but often require extended support systems that may not be available at primarily undergraduate institutions (PUIs). Nevertheless, introducing students to research in this field is critical for preparing the next generation of cognitive neuroscientists.
Despite these challenges, educators have been able to incorporate cognitive neuroscientific methodologies into the undergraduate curriculum, either in simulated (Hurd & Vincent, 2006; Illert et al., 1992; Miller et al., 2008; Mirrione et al., 2014) or actual (de Wit et al., 2017; Nyhus & Curtis, 2016; Wilson, 2006) research experiences involving techniques such as EEG, PET, and fMRI. However, new techniques for understanding the neural basis of cognition are constantly being introduced. For instance, an important methodological development in cognitive neuroscience has been the advent of non-invasive brain stimulation (NIBS; Polanía et al., 2018; Wagner et al., 2007). This group of techniques involves delivering relatively low levels of magnetic pulses or electrical current through the scalp in order to modulate brain function in a temporary manner. The precise method of brain modulation can take a variety of forms, including transcranial magnetic stimulation (TMS), transcranial alternating current stimulation (tACS), and transcranial direct current stimulation (tDCS).
Transcranial direct current stimulation involves the delivery of weak electrical currents (typically in the 1–2 mA range) through saline-soaked sponges positioned over the scalp. Current enters the body through an anodal electrode, which results in a localized increase in neuronal excitability and leaves the body through a separate cathodal electrode, which results in a localized decrease in neuronal excitability (Nitsche & Paulus, 2000). The changes in neuronal excitability typically persist beyond the end of stimulation for a period of minutes to hours, and several recent reviews have confirmed that the technique is a safe and effective method of transiently modulating brain function in a research environment (Bikson et al., 2016; Buchanan et al., 2021; Nikolin et al., 2018).
The use of tDCS in psychological and neuroscientific research has exploded in the last decade. A keyword search of peer-reviewed articles indexed in the MEDLINE database reveals that the terms “tDCS” and “transcranial direct current stimulation” increased by an order of magnitude over the past decade, increasing from 71 publications in 2010 to 820 publications in 2020. Undergraduate teaching resources have also documented this growth. For instance, the three most widely used undergraduate cognitive neuroscience textbooks (Banich & Compton, 2018; Gazzaniga et al., 2018; Ward, 2019) all highlight tDCS as a significant area of increased coverage in their most recent editions, recognizing the growing prominence of this technique within the field.
Despite the increased prevalence of NIBS (and tDCS in particular) within the field of cognitive neuroscience, there has been little effort to incorporate this important new technique into CUREs. In this paper, I describe an advanced undergraduate laboratory course using tDCS that I have successfully implemented at Gettysburg College. The course was a modified version of the fMRI laboratory course that I previously taught (Wilson, 2006), but focused on introducing students to the theoretical and technical basis of non-invasive brain stimulation, and then allowed them to apply this knowledge by designing and implementing their own tDCS projects in small groups. To my knowledge, this is the first CURE using non-invasive brain stimulation to date and demonstrates the feasibility of introducing hands-on NIBS research to the undergraduate psychology and neuroscience curricula.
Course Overview
I implemented this laboratory course in tDCS as a capstone option for Psychology majors at Gettysburg College, a small liberal-arts college in Gettysburg, Pennsylvania. Psychology majors at Gettysburg take two advanced laboratory courses that focus on different subfields in psychology (e.g., developmental psychology, cultural psychology, and in this case, cognitive neuroscience) as their capstone experience. All of the capstone courses focus on the design and implementation of original, student-driven research using discipline-specific methodologies in small groups (typically in groups of 2–3 students).
Course Objectives
The course had four main objectives, namely, (1) to review, analyze, and critique a number of primary research articles spanning multiple methodologies within cognitive neuroscience, (2) to learn about and implement the various steps involved in tDCS research, (3) to reflect on and extend the results of previous empirical research within an area of cognitive neuroscience (using tDCS), and (4) to prepare a manuscript and poster presentation in order to communicate the results of an empirical research project. These objectives are fairly consistent across all of our advanced laboratory courses, namely, to discuss primary literature in a specific subfield and to design and implement original research and then communicate the results of that research using communication standards of the field (i.e., APA-style manuscripts and posters).
Course Prerequisites and Enrollment
Enrollment in each advanced laboratory courses at Gettysburg College is capped at 12 students and these courses share a common prerequisite structure, including Introductory Psychology, a mid-level content course in the relevant subfield (e.g., Cognitive Neuroscience), Statistics, and Experimental Methods. At the time this course was taught, students needed to earn a grade of C or better in Statistics and Methods courses to enroll in any advanced laboratory courses. (The departmental grade requirement for Methods has subsequently been dropped.) Also, there were no restrictions concerning how recently students completed the pre-requisites prior to enrolling in this course. Consequently, there was some variability in terms of when students completed the prerequisite courses. For instance, all of the enrolled students completed Methods either one or two semesters immediately preceding this course. In contrast, students completed Cognitive Neuroscience either in the same academic year, the previous academic year, or in one case two academic years prior to this course.
Course Format
The format of the course closely paralleled the fMRI advanced laboratory course that I have described previously (Wilson, 2006). The course met each week for two 75-minute lecture sessions as well as one three-hour laboratory session. Lecture sessions consisted of a mixture of classes devoted to learning the theoretical and neurophysiological basis of tDCS, as well as classes devoted to reading empirical research articles that employed tDCS to examine specific cognitive processes. Laboratory sessions during the first half of the semester focused on the theoretical and technical bases of conducting tDCS research. During the second half of the semester, those sessions allowed students to design and implement an empirical research project (including data collection and statistical analyses). Materials used in the course, including the full syllabus and examples of video lectures and online learning resources are available online (Wilson, 2021)
Primary Readings
Readings fell into two broad categories: (1) articles focused on tDCS methodology, including the neuromodulatory basis of tDCS (e.g., Nitsche & Paulus, 2000), safety issues (e.g., Bikson et al., 2016), and electrode placement (e.g., DaSilva et al., 2011), and (2) empirical research articles covering a range of topics within cognitive neuroscience (many of which employed tDCS) including working memory (e.g., Berryhill et al., 2010), emotion (e.g., Hortensius et al., 2012), attention (e.g., Schweid et al., 2008), and language (e.g., Flöel et al., 2008). A more extensive list of potential readings is available online (Wilson, 2021) and can be tailored to a prospective instructor’s target audience and course goals.
Transcranial Direct Current Stimulation Hardware
A range of tDCS hardware is available to instructors who would like to incorporate this technology into their courses. Professional-grade systems such as the Activadose II system (https://activatekinc.com/) can cost as little as $400 and are used routinely in neuroscientific research (e.g., Foroughi et al., 2015; Nejati et al., 2021). More expensive systems typically offer additional features such as greater control over sham stimulation, programming modes that allow for double-blinding, and more precise control over current delivery. Mid-range options such as the TCT Research stimulator (https://www.trans-cranial.com/) cost approximately $1000, whereas high-end systems such as the Soterix 1x1 tDCS system (www.soterixmedical.com) can cost upward of $6000. After the initial investment in the tDCS hardware, there are a few ongoing consumable costs, namely, batteries to power the system, saline solution, and disposable sponges that house the stimulating electrodes. Each participant in a tDCS study therefore results in an additional $2–5 in consumables, regardless of the system that is purchased. For this course, I used a Soterix Medical 1x1 tDCS system; however, even the most basic professional-grade system will work well for the purposes of a course-based introduction to non-invasive brain stimulation. As such, an instructor who is not already engaged in tDCS research could realistically develop such an experience after an initial, one-time investment of as little as $500 for the main hardware, with very modest expenditures related to consumables beyond that.
Empirical Research Projects
Students conducted novel research projects using tDCS over the course of the semester in small, self-selected groups (2–3 students per group). Small groups were necessary in part because students needed to share tDCS equipment and laboratory space. Other instructors might prefer larger group sizes or may be able to accommodate a larger number of simultaneous projects, but the need to share tDCS hardware, space, and trained personnel to oversee sessions will most likely be a limiting factor in how many simultaneous projects can be implemented. Each group met with me weekly throughout the semester to discuss their project and to design and implement their study. In all cases, students prepared and submitted an IRB application based on their project and conducted behavioral piloting (without brain stimulation) before implementing the tDCS version of their project. Each group created or acquired their own materials (visual stimuli, surveys, etc.), recruited and screened all participants, implemented their experiment, and analyzed all behavioral data. Students recruited their participants through campus advertising and social media. Participants did not receive monetary compensation for these studies, but in some cases, they were offered a nominal reward (e.g., a candy bar) as a token of appreciation for their time.
I, or a trained research technician from my laboratory, worked with each student group to screen participants, schedule sessions, deliver all electrical stimulation with the tDCS system (i.e., students in the class did not position the electrodes or deliver the electrical current without me or a trained research technician), and conduct post-stimulation symptom interviews to assess any potential adverse effects of tDCS. The students were therefore present and actively engaged during all tDCS sessions to implement the behavioral tasks associated with their project and to participate in the screening, tDCS delivery, and post-stimulation safety protocols. Examples of these safety screening and adverse effect questionnaires are available online (Wilson, 2021) and can easily be modified to accommodate an instructor’s specific needs.
Students were free to choose a topic within cognitive neuroscience that interested them. Their goal was to find existing research that examined the neural basis of a cognitive process using functional brain imaging or non-invasive brain stimulation and then to think of a novel way to extend that result using tDCS. In all cases, students were encouraged to apply commonly used experimental logic for designing tDCS research, for instance, attempting to establish a causal link between brain activity and a cognitive process that has been correlated in past research, assessing the effects of tDCS stimulation montage on a previously documented relationship between brain and behavior, or determining the effects of stimulation polarity (anodal vs. cathodal) on the direction of a previously established relationship between brain activity and cognition.
Student projects took a variety of forms, for instance, one group attempted to establish a causal link between medial prefrontal cortex (MPFC) activity and prosocial behavior (Masten et al., 2011). More specifically, they trained raters to assess the degree of “prosocial” content in emails that were generated by participants who received either anodal or sham tDCS stimulation. Another group attempted to replicate a previous tDCS study of coordinate processing (England et al., 2015) to determine if the previously observed improvements in spatial memory relied on bilateral posterior parietal cortex (PPC) stimulation, or if unilateral stimulation to either hemisphere would produce the same effects. They asked participants to remember the locations of everyday objects embedded in scenes and then assessed differences in spatial memory using the original bilateral stimulation (anodal left; cathodal right), as well as unilateral stimulation (left anodal alone and right cathodal alone).
Discussion
The tDCS laboratory course that I describe here offers a novel approach to introducing undergraduate students to cognitive neuroscience research using non-invasive brain stimulation. The course adds to a growing body of evidence on the effectiveness of offering CUREs involving cognitive neuroscientific methodologies, including functional brain imaging, electroencephalography, and electrophysiology (de Wit et al., 2017; Thibodeau, 2011; Wilson, 2006). This course would make a significant contribution to any undergraduate neuroscience curriculum and would allow instructors and students to develop a working knowledge of a rapidly growing technique for understanding the neural basis of cognition.
Student evaluations were overwhelmingly positive. Many students reported that this course required more time and effort than any of their other courses to date, but that this was also the most fulfilling. Example comments included “This class did spark an interest in research that I didn’t think I would have had without taking the course,” “One of my favorite classes at Gettysburg,” “I am more likely to read neuro [science] articles for fun,” and “Working with tDCS is great because it’s new and interesting. I may never get to do it again, so I think it was a great opportunity.” In light of the very small sample size, and the inability to directly compare learning outcomes for this course with other non-tDCS courses, it is important to recognize that this evidence is anecdotal, and that additional work is needed to quantify the potential benefits of a tDCS laboratory course relative to other neuroscience-based CUREs.
Despite the potential benefits of a tDCS laboratory course, there are several potential limitations that must be noted. One relates to the cost of developing and implementing such a course. Conducting tDCS research does require an initial hardware investment that can be cost-prohibitive for some individual faculty or institutions. However, tDCS systems cost significantly less than other commonly used research methodologies in cognitive neuroscience such as fMRI and EEG and therefore are much easier to acquire, especially for researchers at PUIs. Moreover, for instructors who are already engaged in tDCS research, the added costs of implementing this technology into a CURE are minimal.
A second concern of implementing such a course relates to the safety of tDCS. A wide range of review and meta-analyses confirm that tDCS is a safe and effective method of modulating brain function (Bikson et al., 2016; Buchanan et al., 2021; Nikolin et al., 2018) if researchers adhere to accepted protocols concerning the recruitment of participants, the delivery of stimulation, and the monitoring of potential adverse effects (AEs). Course instructors, graduate students, research/teaching assistants, etc. can all oversee the implementation of tDCS research after receiving basic safety training. Such training typically involves reading and reviewing several articles concerning the mechanisms and safety of non-invasive brain stimulation, shadowing an experienced tDCS researcher, and then having the trainee conduct their own supervised sessions with feedback. Such a program only requires a few weeks and does not involve any additional costs. Alternatively, a small number of fee-based training courses exist, both online (e.g., https://lms.neurocademy.com/courses/an-introduction-to-tdcs/) and in-person; however, the COVID-19 pandemic has halted many of these in-person training workshops. If the personnel overseeing the process at each stage have received adequate training and adhere to standard operating procedures (Antal et al., 2017), then there should not be any significant concerns related to incorporating this form of NIBS into the undergraduate curriculum.
One final limitation worth mentioning relates to the fact that there is still considerable debate about the efficacy of non-invasive brain stimulation on cognition, in general. Several recent reviews (Horvath et al., 2015; Medina & Cason, 2017) suggest that the modulatory effects of tDCS on cognition are modest and that such effects are often difficult to replicate given the typically small sample sizes used in such studies (Minarik et al., 2016). As a result, a course-based research experience involving tDCS, which will likely be under-powered, may be more likely to generate false negative results compared to other neuroscientific research methodologies.
In summary, an advanced undergraduate laboratory course in tDCS is possible and has the potential to provide students with a novel method of engaging directly in cognitive neuroscience research using an important, and increasingly more common, methodology. Students in this course designed and conducted original tDCS research under close supervision and while additional work is necessary to formally assess the benefits of this experience on student learning, their evaluations provided anecdotal evidence suggesting that it was a positive experience. For undergraduate instructors, particularly those at PUIs, this might represent a cost-effective method of engaging students directly in cognitive neuroscience research within the undergraduate curriculum.
Footnotes
Declaration of Conflicting Interests
The author declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
The author received no financial support for the research, authorship, and/or publication of this article.
