prior to the study , fourteen brain regions were identified for which location on a diagram ( term a ) , name ( term b ) , and function ( term c ) were regularly taught and tested within the course ( table 1 ) . fourteen ab and bc conditional relations were then explicitly taught throughout three lectures using powerpoint slides . for seven of these 14 regions , the ac transitive relation was also explicitly taught ( last column of table 1 ) . the relations taught in lecture were also provided on study guides , which , along with the powerpoint lectures , were available to the students on the first day of class . all students queried reported studying from the study guides and powerpoint presentations prior to the test . on the exam , all of the directly - taught relations were assessed as well as two relations that , based on an ebi paradigm , should emerge in the absence of direct training . the emergent relations were the symmetrical relations  does cb ?  and transitive relations ninety - three undergraduates were enrolled in a semester - long , introductory level behavioral neuroscience course that met once per week for a 3-hour lecture . the class included freshmen through seniors , 63 females and 30 males , and consisted predominantly of psychology majors ( 56.6% ) , followed by undeclared majors ( 23% ) , neuroscience majors ( 5.7% ) , biology majors ( 3.4% ) , and other ( 11.3% ) . teaching and testing stimuli involved 14 brain regions and the following characteristics : a ) brain location on a diagram , b ) the name of the brain region , and c ) a particular function of the brain region ( table 1 ) . ab and bc relations were taught for all regions . ac was explicitly taught for seven of the 14 regions , identified in table 1 , last column . because the study was embedded within an existing course , we did not change the course material in order to test for specific emergent relations . we selected three lecture topics to use as the basis for the experiment : emotion , brain rhythms , and memory systems . the lectures corresponded to the text neuroscience : exploring the brain ( bear et al . , 2007 ) chapters 18 , 19 , and 24 , respectively . our criteria for selecting brain location - name - function relations used in this study were : 1 ) those that students specifically had demonstrated difficultly with in previous semesters , and 2 ) those that students were unlikely to know already from past courses or general knowledge . for instance , a substantial component of the lecture on memory systems is devoted to understanding the role of the hippocampus in memory formation : in hippocampal - dependent types of learning , in spatial memory ( including a discussion of place cells ) , and in relational memory . given the emphasis on these structure - function relations in class , the majority of students in past semesters were successful in answering exam questions about the roles of the hippocampus in learning and memory . therefore , we excluded these relations from the present study anticipating a ceiling effect . instead , for the hippocampus , we targeted a topic that was less well known , but nonetheless was normally covered in the emotion lecture of the course : the brain regions and functions of the papez circuit , as presented by bear et al . , ( 2007 , see also shah et al . , 2012 ) . in the text , the papez circuit is shown as a schematic diagram ( boxes and arrows ) and also in a brain diagram along with a simple emotion - related function associated with each region . the papez circuit diagram was taught in the context of discussing whether there was more anatomical evidence for the cannon - bard model of emotion or the james - lange model . papez proposed that the hippocampus was involved in emotion because it is one of the central targets of rabies infection , resulting in hyperemotional responses and expressions of fear and aggression ( bear et al . we chose to include this relation in the ebi study , within the historical context of papez s proposition . two other regions of the papez circuit were also used : the neocortex and the anterior nuclei of the thalamus . regions of the neocortex that are interconnected with the cingulate cortex are described by bear et al . , ( 2007 ) as providing  emotional coloring  of emotional experiences ( see also mriau et al . , 2006 ) . thus , we selected  enriches and fine tunes emotional experience  modified from bear et al . ( 2007 ) as the particular function of the neocortex that we tested with ebi . papez also suggested that the anterior thalamus contributed to emotional expression , based largely on anatomical connections within papez s circuit ( review in armstrong , 1990 ) . case studies report that lesions of the anterior nucleus of the thalamus lead to emotional disorders such as spontaneous laughing and crying ( presented in bear et al . , 2007 ) . in keeping with the text , the description of the papez neural pathway was followed by a discussion of criticisms of the models of both the papez circuit and the limbic system in describing a single  emotional system .  in selecting brain structure - function relations presented within the memory systems lecture and text chapter , past semesters have demonstrated that it was more difficult for students to learn brain regions outside the medial temporal lobe that function in declarative memory formation , than to learn associations between memory and temporal lobe regions as noted above . for this reason , we selected the stimuli of the anterior and dorsomedial nuclei of the thalamus and the mammillary bodies and their functions in declarative memory formation ( e.g. , mitchell and dalrymple - alford , 2006 ) . this patient was speared through the left dorsomedial thalamus while fencing and suffered anterograde amnesia ( squire and moore , 1979 ; pinel , 1993 ) . to test the ebi strategy , we used only the term  thalamus  in pairing with the role in memory formation , rather than the specific nuclei , because the specific names of the anterior and dorsomedial nuclei were not normally taught or tested in association with memory in this introductory level class . the mammillary bodies of the diencephalon and the pathway of the fornix contribute to declarative memory formation and damage to the mammillary bodies can be caused by extreme thiamine deficiency as occurs in wernicke - korsakoff syndrome , resulting in anterograde amnesia ( pinel , 1993 ) . likewise , other brain region functions shown here as stimuli were used in the context of assessing the success of ebi . for instance , the striatum is presented here in the context of memory systems , and other functions of the striatum taught in the course are not listed in the table and were not included in the ebi evaluation . carefully controlled teaching presentations of these particular relations between brain location , name , and associated function allowed us to increase the likelihood that the emergent relations we observed in testing did not arise from exposure to the non - taught relations in other contexts outside of the course or in other areas throughout the course . two test sections were administered sequentially in one sitting : part 1 , which had two versions , and part 2 , which was identical for all students . part 1 ( 72 questions ) was completed and turned in before beginning part 2 ( 14 questions ) . first , we assessed the relations that were explicitly taught in class : ab ( 14 questions , brain regions 114 shown in table 1 ) and bc ( seven pairs in version 1 and seven different bc pairs in version 2 , 14 pairs total ) . questions testing ab relations provided a diagram with the anatomical region highlighted ( a ) and five potential region names ( b ) . questions examining bc relations provided the brain name ( b ) in the question and functions ( c ) were provided as choices . for instance , one bc question asked : if the striatum is damaged , this will impair the ability to a ) direct eye movements to a visual cue that is no longer present , b ) associate a fearful stimulus with a certain location , c ) learn a motor behavior used in forming a procedural memory , d ) learn to navigate a new town , e ) remember a phone number while dialing . the correct answer is c. correct responses to both ab and bc questions for a given brain region were the criteria for determining whether to include an individual student s response to the non - taught transitive test in part 2 : does ac ? for example , the question cb ( matched to the bc example above ) , was : learning a motor behavior used in forming a procedural memory requires the : a ) lateral intraparietal cortex , b ) amygdala , c ) striatum , d ) hippocampus , e ) prefrontal cortex . the correct answer is c. the two versions of part 1 differed in whether a given brain region was presented as bc or cb . across both versions , all 14 brain regions were presented in both formats . in version 1 , the bc format was used for the odd numbered brain regions in table 1 ( n=7 ) and cb was used for the even numbered brain regions ( n=7 ) . in version 2 , this ensured that question formats were roughly evenly distributed across the lecture topics . to determine whether students demonstrated non - taught symmetry , we compared the mean percentage of correct answers to bc and cb , matched to brain region and function . this was a between - subject analysis because each student received only one question relating name to function ( in one of the two formats ) for each brain region . if symmetrical relations emerged , we would expect no difference in performance between bc and cb questions . part 2 consisted of a series of diagrams with 14 brain regions highlighted , one per question . each question had five choice options for the function of the region , i.e. , a ( diagram )  c ( function ) . seven of the brain location - function pairs had been explicitly taught in class , seven had not been taught . for transitive relations that had not been taught , we assessed whether the number of correct responses to ac differed from chance to determine whether ac equivalence occurs in the absence of explicit teaching . next , we compared the numbers of correct responses between these two sets of a c questions ( taught and non - taught ) to determine whether explicitly teaching ac improves performance . as noted above , responses to ac questions were noted as correct or incorrect only for students who had correct answers to ab and bc questions for the corresponding brain region . the criterion was put in place because previous laboratory research suggests that without mastery of these relations one would not expect ac relations to emerge . we used a paired t - test to compare percentage correct answers for bc and the complementary cb ( matched to brain region and function , between students ) . of the ac pairs that met criteria ( ab and bc were mastered ) we compared the numbers of correct answers and incorrect answers for the taught and non - taught ac pairs using a chi squared test . we also determined whether the non - taught ac and cb pairs were answered correctly significantly more than chance using a binomial test . prior to the study , fourteen brain regions were identified for which location on a diagram ( term a ) , name ( term b ) , and function ( term c ) were regularly taught and tested within the course ( table 1 ) . fourteen ab and bc conditional relations were then explicitly taught throughout three lectures using powerpoint slides . for seven of these 14 regions , the ac transitive relation was also explicitly taught ( last column of table 1 ) . the relations taught in lecture were also provided on study guides , which , along with the powerpoint lectures , were available to the students on the first day of class . all students queried reported studying from the study guides and powerpoint presentations prior to the test . on the exam , all of the directly - taught relations were assessed as well as two relations that , based on an ebi paradigm , should emerge in the absence of direct training . the emergent relations were the symmetrical relations  does cb ?  and transitive relations ninety - three undergraduates were enrolled in a semester - long , introductory level behavioral neuroscience course that met once per week for a 3-hour lecture . the class included freshmen through seniors , 63 females and 30 males , and consisted predominantly of psychology majors ( 56.6% ) , followed by undeclared majors ( 23% ) , neuroscience majors ( 5.7% ) , biology majors ( 3.4% ) , and other ( 11.3% ) . teaching and testing stimuli involved 14 brain regions and the following characteristics : a ) brain location on a diagram , b ) the name of the brain region , and c ) a particular function of the brain region ( table 1 ) . ab and bc relations were taught for all regions . ac was explicitly taught for seven of the 14 regions , identified in table 1 , last column . because the study was embedded within an existing course , we did not change the course material in order to test for specific emergent relations . we selected three lecture topics to use as the basis for the experiment : emotion , brain rhythms , and memory systems . the lectures corresponded to the text neuroscience : exploring the brain ( bear et al . , 2007 ) chapters 18 , 19 , and 24 , respectively . our criteria for selecting brain location - name - function relations used in this study were : 1 ) those that students specifically had demonstrated difficultly with in previous semesters , and 2 ) those that students were unlikely to know already from past courses or general knowledge . for instance , a substantial component of the lecture on memory systems is devoted to understanding the role of the hippocampus in memory formation : in hippocampal - dependent types of learning , in spatial memory ( including a discussion of place cells ) , and in relational memory . given the emphasis on these structure - function relations in class , the majority of students in past semesters were successful in answering exam questions about the roles of the hippocampus in learning and memory . therefore , we excluded these relations from the present study anticipating a ceiling effect . instead , for the hippocampus , we targeted a topic that was less well known , but nonetheless was normally covered in the emotion lecture of the course : the brain regions and functions of the papez circuit , as presented by bear et al . , in the text , the papez circuit is shown as a schematic diagram ( boxes and arrows ) and also in a brain diagram along with a simple emotion - related function associated with each region . the papez circuit diagram was taught in the context of discussing whether there was more anatomical evidence for the cannon - bard model of emotion or the james - lange model . papez proposed that the hippocampus was involved in emotion because it is one of the central targets of rabies infection , resulting in hyperemotional responses and expressions of fear and aggression ( bear et al . we chose to include this relation in the ebi study , within the historical context of papez s proposition . two other regions of the papez circuit were also used : the neocortex and the anterior nuclei of the thalamus . regions of the neocortex that are interconnected with the cingulate cortex are described by bear et al . , ( 2007 ) as providing  emotional coloring  of emotional experiences ( see also mriau et al . , 2006 ) . thus , we selected  enriches and fine tunes emotional experience  modified from bear et al . ( 2007 ) as the particular function of the neocortex that we tested with ebi . papez also suggested that the anterior thalamus contributed to emotional expression , based largely on anatomical connections within papez s circuit ( review in armstrong , 1990 ) . case studies report that lesions of the anterior nucleus of the thalamus lead to emotional disorders such as spontaneous laughing and crying ( presented in bear et al . , 2007 ) . in keeping with the text , the description of the papez neural pathway was followed by a discussion of criticisms of the models of both the papez circuit and the limbic system in describing a single  emotional system .  in selecting brain structure - function relations presented within the memory systems lecture and text chapter , past semesters have demonstrated that it was more difficult for students to learn brain regions outside the medial temporal lobe that function in declarative memory formation , than to learn associations between memory and temporal lobe regions as noted above . for this reason , we selected the stimuli of the anterior and dorsomedial nuclei of the thalamus and the mammillary bodies and their functions in declarative memory formation ( e.g. , mitchell and dalrymple - alford , 2006 ) . in the lecture , the case study of  n.a . this patient was speared through the left dorsomedial thalamus while fencing and suffered anterograde amnesia ( squire and moore , 1979 ; pinel , 1993 ) . to test the ebi strategy , we used only the term  thalamus  in pairing with the role in memory formation , rather than the specific nuclei , because the specific names of the anterior and dorsomedial nuclei were not normally taught or tested in association with memory in this introductory level class . the mammillary bodies of the diencephalon and the pathway of the fornix contribute to declarative memory formation and damage to the mammillary bodies can be caused by extreme thiamine deficiency as occurs in wernicke - korsakoff syndrome , resulting in anterograde amnesia ( pinel , 1993 ) . likewise , other brain region functions shown here as stimuli were used in the context of assessing the success of ebi . for instance , the striatum is presented here in the context of memory systems , and other functions of the striatum taught in the course are not listed in the table and were not included in the ebi evaluation . carefully controlled teaching presentations of these particular relations between brain location , name , and associated function allowed us to increase the likelihood that the emergent relations we observed in testing did not arise from exposure to the non - taught relations in other contexts outside of the course or in other areas throughout the course . two test sections were administered sequentially in one sitting : part 1 , which had two versions , and part 2 , which was identical for all students . part 1 ( 72 questions ) was completed and turned in before beginning part 2 ( 14 questions ) . first , we assessed the relations that were explicitly taught in class : ab ( 14 questions , brain regions 114 shown in table 1 ) and bc ( seven pairs in version 1 and seven different bc pairs in version 2 , 14 pairs total ) . questions testing ab relations provided a diagram with the anatomical region highlighted ( a ) and five potential region names ( b ) . questions examining bc relations provided the brain name ( b ) in the question and functions ( c ) were provided as choices . for instance , one bc question asked : if the striatum is damaged , this will impair the ability to a ) direct eye movements to a visual cue that is no longer present , b ) associate a fearful stimulus with a certain location , c ) learn a motor behavior used in forming a procedural memory , d ) learn to navigate a new town , e ) remember a phone number while dialing . the correct answer is c. correct responses to both ab and bc questions for a given brain region were the criteria for determining whether to include an individual student s response to the non - taught transitive test in part 2 : does ac ? for example , the question cb ( matched to the bc example above ) , was : learning a motor behavior used in forming a procedural memory requires the : a ) lateral intraparietal cortex , b ) amygdala , c ) striatum , d ) hippocampus , e ) prefrontal cortex . the correct answer is c. the two versions of part 1 differed in whether a given brain region was presented as bc or cb . across both versions , the bc format was used for the odd numbered brain regions in table 1 ( n=7 ) and cb was used for the even numbered brain regions ( n=7 ) . in version 2 this ensured that question formats were roughly evenly distributed across the lecture topics . to determine whether students demonstrated non - taught symmetry , we compared the mean percentage of correct answers to bc and cb , matched to brain region and function . this was a between - subject analysis because each student received only one question relating name to function ( in one of the two formats ) for each brain region . if symmetrical relations emerged , we would expect no difference in performance between bc and cb questions . part 2 consisted of a series of diagrams with 14 brain regions highlighted , one per question . each question had five choice options for the function of the region , i.e. , a ( diagram )  c ( function ) . seven of the brain location - function pairs had been explicitly taught in class , seven had not been taught . for transitive relations that had not been taught , we assessed whether the number of correct responses to ac differed from chance to determine whether ac equivalence occurs in the absence of explicit teaching . next , we compared the numbers of correct responses between these two sets of a c questions ( taught and non - taught ) to determine whether explicitly teaching ac improves performance . as noted above , responses to ac questions were noted as correct or incorrect only for students who had correct answers to ab and bc questions for the corresponding brain region . the criterion was put in place because previous laboratory research suggests that without mastery of these relations one would not expect ac relations to emerge . we used a paired t - test to compare percentage correct answers for bc and the complementary cb ( matched to brain region and function , between students ) . of the ac pairs that met criteria ( ab and bc were mastered ) we compared the numbers of correct answers and incorrect answers for the taught and non - taught ac pairs using a chi squared test . we also determined whether the non - taught ac and cb pairs were answered correctly significantly more than chance using a binomial test . there was no difference in mean scores between students who took part 1 version 1 ( n=47 , mean=72.8%  2.174 , range 4397% ) and students who took part 1 version 2 ( n=46 , mean=71.9%  2.975 , range 4198% ) ( t - test , t=1.19 , 2-tailed p=0.261 ) , demonstrating that both versions were of similar overall difficulty . all students took the same test for part 2 ( n=93 , mean=71.39%  31.860 , range=41100% ) . the 14 explicitly taught bc questions were then graded for each student independent of the rest of the exam questions . on these questions , fewer correct responses were given to cb questions compared with the respective bc questions for the same brain regions ( figure 1 , paired t - test on numbers ( not percentages ) of correct answers , t=3.420 , p=0.008 ) . however , cb questions were answered correctly significantly more than the chance value of 20% ( binomial , p<0.05 ) . for each student we then identified the brain regions for which they correctly answered both ab and bc questions relating to that region . for these regions only , we calculated the number of ac questions that were answered correctly . this resulted in a total of 636 ac pairs across all students exams ( range 214 qualifying ac questions per student ) . answers to ac pairs were not further divided into within - student or within - topic levels . we grouped all ac questions that were explicitly taught across students and topics and separately grouped all ac questions that were not explicitly taught . we found that ac performance for non - taught brain relations was 83.33% , significantly better than the chance value of 20% , binomial test , p<0.001 , p=.2 , q=.8 , figure 2 ) , demonstrating the emergence of ac equivalence . we next asked whether teaching the ac equivalence improved performance above that which emerged spontaneously . for the 318 explicitly taught ac pairs , 272 ( 85.53% ) were answered correctly and 46 ( 14.47% ) answered incorrectly . for the 318 non - taught ac pairs , 260 were answered correctly ( 81 . there was no difference in distribution of correct and incorrect responses between equivalence pairs that were taught and those that were not ( =0.27 , df = 1 , p=0.603 ) . therefore , teaching the ac equivalence between brain location on a diagram and function of the region did not improve performance on the exam . this study reports evidence of the transportability of ebi to a natural classroom environment . previous research using ebi has been conducted under tightly controlled conditions and results have suggested that this paradigm may have implications for more traditional teaching practices ( e.g. , fienup et al . , 2010 ) . the current study verifies the utility of the paradigm in designing college - level lecture instruction of neuroanatomy . overall , these results support the notion that the ebi paradigm can be used as a model for planning which relations to teach explicitly and which are likely to emerge without direct training . the implications are that instructors can more efficiently plan what is taught and use time saved to increase the amount of information covered in a course . functional neuroanatomy in this course has historically been taught without regard to balancing the abc information for all brain regions covered in the content . the locations of brain regions are normally shown on diagrams while introducing the name of the region ( ab and ba ) . we have only recently begun to explicitly teach ac , by showing a diagram and questioning the class  what does this region do ?  in part , this was begun in a deliberate effort by the instructor to better engrain the material by creating more associations or  links  within brain region sets or categories . however , the ac teaching was not systematic and was not presented for every brain region . the utility of teaching ac , and the question of whether to comprehensively teach all ab , bc , ac relations prompted this study . a few studies have examined the utility of this paradigm with students enrolled in a course , learning course - related material ; however , the ebi was separated from the actual classroom teaching . 2011 ) taught students enrolled in a research methods course about inferential statistics and hypothesis decision making . this study compared the effects of no - instruction , ebi instruction , and the performance of a group of students who learned all possible relations ( including formal training on symmetrical , transitive , and equivalence relations ) . similar to the results found here , ebi was as effective as learning all relations , but required less formal training . however , instruction was computer based and conducted in a relatively distraction - free setting . because the present study took place within the context of a natural course context , we did not control for student behavior . in computer driven laboratory studies of ebi , participants are not allowed to take notes or  study   the computer program teaches overlapping relations immediately followed by a test of the whole concept . in the present study in fact , some portion of students may have studied the seven ac relations that were not directly trained . however , regardless of whether the ac relations emerged during the test or in the course of studying , test performance demonstrates that an instructor can model teaching behaviors on the ebi paradigm and expect new associations to be demonstrated . an interesting finding was that there was a significantly greater number of correct responses to bc than the non - taught symmetrical variant cb , although cb answers were correct more often than predicted by chance . the result might be explained by the type of stimuli : names and functions . a recent basic study found that classes of familiar stimuli are more likely to form equivalence classes than unfamiliar stimuli ( fields et al . , in press ) . in the current study , brain names may be more familiar than functions ; and therefore , it could be that the particular stimuli influence the outcomes . in addition , the direction of training ( ab , bc v. ab , ac ) may impact concept formation ( arntzen and holth , 1997 ) . a number of basic ( e.g. , adams et al . , 1993 ; arntzen and holth , 1997 ) and applied ( fienup and critchfield 2011 ) studies have shown that full concepts , based on an ebi paradigm , do not always emerge as planned . research in this area has begun to look at different instructional components that influence the spontaneous formation of new associations ( for a review , see fienup , et al . , 2011 ) . according to mathematical set theory , familiarity with stimuli and direction of training should not influence ebi and concept formation , but the data examining these issues point in a different direction . in sum , a number of factors could have influenced the differences in responding to bc and cb relations and ebi research has yet to provide an explanation for discrepancies of this sort . laboratory studies of ebi have demonstrated that a large number of non - taught equivalence associations may emerge spontaneously as concepts are formed and merged . for instance , fienup and critchfield ( 2010 ) taught 40 statistics relations and generated 144 total emergent relations , a total of 4.7 times as many relations as had been directly taught . in the present study , although we taught and assessed fewer relations , it is easy to see how additional information can be added as stimuli to anatomical sets thereby increasing the amount of spontaneously emergent equivalences . for instance , we taught brain location on a diagram , region name , and a single function . additional relevant stimuli could be included such as : multiple functions , a disease or disorder that targets that region ( or the disorder resulting from damage to the region ) , the name of a case study giving rise to our understanding of the region , the neurotransmitter(s ) used in that region , projections to / from the region , functional and/or anatomical subdivisions within the region . as the complexity of relations increases , so does the number of expected emergent relations , thus increasing efficiency in teaching . for instance , a set for understanding how sound intensity is encoded in action potential firing may include : increasing sound volume  increased displacement of the oval window  increased basilar membrane wave amplitude  increased bending of hair cell cilia  increased depolarization  higher rate of action potentials . here we have abcdef . as in fienup and critchfield ( 2010 ) teaching targeted relations would be expected to result in multiple emergent relations : e.g. , increased bending of hair cell cilia results in a higher rate of action potentials ( df ) . use of ebi requires that the instructor identify the information belonging to a set ahead of the lecture , determine which relationships to teach , and emphasize those pairs in class and on any of the presentation materials such as slides , study guides , and test question banks . to our knowledge the current study is the first to use ebi within the natural teaching and testing context of an undergraduate course . these results demonstrate that ebi may be a valuable strategy to focus teaching time on carefully selected associations between elements of a conceptual class in order to encourage larger concept formation . in particular , ebi may be particularly valuable in large classes in which instructors do not receive individual feedback on whether students master all individual associations taught . therefore , by balancing redundancy in teaching relations among stimuli within a set with efficiency of not teaching all associations , instructors may aim to maximize the emergence of complete concepts while maintaining efficiency in time allocation .
a goal of all instruction is to efficiently allocate time spent teaching -- balancing redundancy that enhances learning with redundancy that is irrelevant to increasing student understanding . 
 efficient allocation of time allows the instructor to present additional material and go into more detail about the information being presented . 
 here we borrow laboratory research on concept formation and apply these formal principles in teaching introductory neuroanatomy within a lecture course on behavioral neuroscience . 
 concept formation is taught by pairing multiple stimuli , for instance brain name , location , and function , in such a way that novel associations within a category emerge without direct training . 
 this study demonstrates that careful selection of associations by the instructor can encourage the spontaneous emergence of novel associations within a concept or category , thereby increasing efficiency of teaching and by extension , the depth of material that can be taught .