Abstract

Human imitation is supported by an underlying “mirror system” principally composed of inferior frontal, inferior parietal, and superior temporal cortical regions. Across primate species, differences in frontoparietotemporal connectivity have been hypothesized to explain phylogenetic variation in imitative abilities. However, if and to what extent these regions are involved in imitation in nonhuman primates is unknown. We hypothesized that “Do As I Do” (DAID) imitation training would enhance white matter integrity within and between frontoparietotemporal regions. To this end, four captive chimpanzees (Pan troglodytes) were trained to reproduce 23 demonstrated actions, and four age-/sex-matched controls were trained to produce basic husbandry behaviors in response to manual cues. Diffusion tensor images were acquired before and after 600 min of training over an average of 112 days. Bilateral and asymmetrical changes in frontoparietotemporal white matter integrity were compared between DAID trained subjects and controls. We found that imitation trained subjects exhibited leftward shifts in both mean fractional anisotropy and tract strength asymmetry measures in brain regions within the mirror system. This is the first report of training-induced changes in white matter integrity in chimpanzees and suggests that frontoparietotemporal connectivity, particularly in the left hemisphere, may have facilitated the emergence of increasingly complex imitation learning abilities.

INTRODUCTION

Imitation is defined as the transformation of others' actions into one's own (modified from Thorndike, 1898). Many have hypothesized that learning by imitation plays an important role in social cognition and cultural variation in human behavior. From birth, humans imitate facial expressions (Meltzoff & Moore, 1977), and by 9’months of age, they engage in imitative play (Meltzoff, 1990). Throughout development and adulthood, humans learn about their social and physical environment by observing and imitating others' actions (Heyes, 1993). Imitative abilities are associated with a large suite of human sociocognitive processes such as empathy (Williams, Nicolson, Clephan, de Grauw, & Perrett, 2013; Iacoboni, 2009; Pfeifer, Iacoboni, Mazziotta, & Dapretto, 2008; Schulte-Ruther, Markowitsch, Fink, & Piefke, 2007; Carr, Iacoboni, Dubeau, Mazziotta, & Lenzi, 2003), joint attention (Charman et al., 1997; Carpenter, Tomasello, & Savagerumbaugh, 1995), mirror self-recognition (Nielsen & Dissanayake, 2004; Asendorpf, Warkentin, & Baudonnière, 1996), and action/intention understanding (Rizzolatti & Fogassi, 2014). Furthermore, imitation's role in human social learning likely underlies cultural transmission of specific behavior patterns (Whiten, McGuigan, Marshall-Pescini, & Hopper, 2009) including language (Corballis, 2010; Iacoboni, 2009; Iacoboni & Wilson, 2006; Rizzolatti & Craighero, 2004; Nadel, 2002). These collective findings have led some to assert that imitation is what distinguishes humans from other species (Meltzoff, 1988).

To what extent imitative abilities are uniquely human is a matter of considerable debate (Buttelmann, Carpenter, Call, & Tomasello, 2013; Tennie, Call, & Tomasello, 2012; Visalberghi & Fragaszy, 2002; see also Galef, 2012, for a review of social learning across animal taxa). Some have suggested that truly imitative behaviors are nonexistent in nonhuman primates (Tennie, Call, & Tomasello, 2009; Tomasello, 1996; Tomasello, Kruger, & Ratner, 1993); however, a large body of evidence indicates considerable similarities between apes' and humans' imitative capacities (see Whiten, 2017, for a review). Like human infants, there is evidence that newborn chimpanzees can imitate some facial expressions (Bard, 2007; Myowa-Yamakoshi, Tomonaga, Tanaka, & Matsuzawa, 2004), and similar findings have been reported in some macaque species (Paukner, Pedersen, & Simpson, 2017; Paukner, Simpson, Ferrari, Mrozek, & Suomi, 2014). There is also evidence of species differences in imitation recognition and production abilities. For instance, the ability to recognize when one is being imitated is present in all great apes that have been tested to date (Pope, Russell, & Hopkins, 2015; Haun & Call, 2008; Nielsen & Dissanayake, 2004; Asendorpf et al., 1996) but is equivocal in Old and New World monkeys (Paukner, Suomi, Visalberghi, & Ferrari, 2009; Paukner, Anderson, Borelli, Visalberghi, & Ferrari, 2005). This imitation recognition likely relies, at least in part, on neural networks that also serve imitation production.

Humans tend to copy the specific actions used during a demonstration, even irrelevant ones (Horner & Whiten, 2005), whereas chimpanzees tend to reproduce the end-state of demonstrations, ignoring the details of the actions (Carpenter & Call, 2009; Buttelmann, Carpenter, Call, & Tomasello, 2007; Tennie, Call, & Tomasello, 2006; Call, Carpenter, & Tomasello, 2005; Myowa-Yamakoshi & Matsuzawa, 2000); yet importantly, they are capable of invoking more specific action-copying (Horner & Whiten, 2005). Indeed, evidence has shown that apes can learn to play a “Do As I Do” (DAID) imitation game, in which they reproduce demonstrated actions during a training period and then continue to imitate when tested with a battery of novel actions (Call, 2001; Custance, Whiten, & Bard, 1995; Hayes & Hayes, 1952). In contrast, attempts to teach monkeys this same imitation game have been largely unsuccessful and seem to suggest that they may favor end-state copying by mimicking the environmental effect of demonstrations, rather than copying others' specific actions (Fragaszy, Deputte, Cooper, Colbert-White, & Hemery, 2011; Visalberghi & Fragaszy, 2002; Mitchell & Anderson, 1993). In fact, when action-copying is irrelevant, monkeys' ability to learn an abstract response sequence is facilitated by observing a conspecific; a process termed cognitive imitation (Subiaul, Cantlon, Holloway, & Terrace, 2004). Thus, the extent to which action- versus goal-copying behaviors are utilized varies considerably within the primate lineage.

In the current study, we sought to examine the neural basis of imitation in chimpanzees. If and to what extent the human imitative phenotype relies on the same neural substrates as other primates' action-copying behaviors is controversial (Hickok, 2009). The discovery of mirror neurons, which fire both when an action is produced and when the same action (produced by another individual) is observed, within the macaque premotor area F5, has been hypothesized to be a critical neuronal mechanism involved in action-copying (Gallese, Fadiga, Fogassi, & Rizzolatti, 1996; di Pellegrino, Fadiga, Fogassi, Gallese, & Rizzolatti, 1992). Additional mirror neurons were later found within monkey parietal regions, which innervate the premotor cortex (Gallese, Fadiga, Fogassi, & Rizzolatti, 2002). With the incorporation of superior temporal regions, which are involved in recognizing biological motion (Perrett et al., 1990) and are reciprocally connected to parietal regions, a putative macaque imitation system has emerged (Rizzolatti, Fogassi, & Gallese, 2002; Gallese et al., 1996). However, one significant limitation of the mirror neuron system model of imitation in macaque monkeys is the simple fact that the available data indicate that the imitative abilities of species within this genus are notably limited (Visalberghi & Fragaszy, 2002).

In humans, imitation also involves frontoparietotemporal regions. In keeping with the existing nomenclature, we refer to these regions collectively as the putative “mirror system” throughout the text; this should not be taken as an indication that it is necessarily composed of mirror neurons (see Hickok, 2009, for a critical discussion of the “mirror neuron system”). During imitation, an action is observed, translated into a mental representation (including its goal, if known), and then transformed into the observer's own action. Similar to monkeys, in humans the STS is implicated in the initial observation of bodily motion (Allison, Puce, & McCarthy, 2000), and it is reciprocally connected to the inferior parietal lobule (IPL), which appears to be involved in coding an observed action's valence and direction (Fabbri-Destro & Rizzolatti, 2008; Halsband et al., 2001; Goldenberg, 1999). The IPL, in turn, is connected to frontal mirror regions, namely within the inferior frontal gyrus (IFG), which functions in goal imitation (Hecht et al., 2013; Koski et al., 2002; Iacoboni et al., 1999).

To explain the spectrum of primate imitative phenotypes, Hecht et al. (2013) compared frontoparietotemporal white matter connectivity among macaques, chimpanzees, and humans. These authors found prominent ventral STS to IPL connections in macaques, pronounced dorsal IPL to IFG connections in humans, and more equivalently proportioned dorsal/ventral connections in chimpanzees. According to Hecht et al. (2013), ventral connections, hypothesized to facilitate the understanding of actions' goals, underlie macaques' goal-copying, whereas dorsal connections, hypothesized to facilitate the understanding of action kinematic details, underlie humans' action-copying abilities. Thus, chimpanzees' intermediate expression of both dorsal and ventral connections is consistent with their intermediate usage of both goal- and action-copying. Although there appears to be homology between the macaque and human frontoparietotemporal systems, its functional involvement in chimpanzee imitation is entirely speculative. Indeed, there are no data regarding the functional correlates of imitation in chimpanzees or other great apes; thus, the hypothesis that the same frontoparietotemporal regions are involved in ape imitation remains untested.

As a means of examining the potential neural basis of imitation in chimpanzees, the current study utilized diffusion tensor imaging (DTI) before and after DAID imitation training to assess changes in frontoparietotemporal connectivity. DTI has been used in humans to document training-induced cortical changes for numerous motor and cognitive tasks, such as juggling (Scholz, Klein, Behrens, & Johansen-Berg, 2009), second language acquisition (Schlegel, Rudelson, & Tse, 2012), and playing an instrument (Zatorre, Fields, & Johansen-Berg, 2012; Hyde et al., 2009). In addition, chimpanzees are capable of being taught the DAID imitation game and subsequently apply the “copy this” rule to successfully imitate novel actions (Custance et al., 1995; Hayes & Hayes, 1952). Here, we combined DAID imitation training with DTI scanning to quantify changes in cortical connectivity, specifically within the frontoparietotemporal mirror system. After learning the imitation game, we measured chimpanzees' imitative abilities on a list of novel actions (i.e., not part of their training). We hypothesized that if IFG, IPL, and STS regions are involved in imitation in chimpanzees, then connectivity between these putative mirror regions would increase following successful DAID imitation game acquisition and participation.

METHODS

Subjects

Eight adult captive chimpanzees, four male and four female, housed at the Yerkes National Primate Research Center (YNPRC) were matched on sex, rearing history, age (within 6 years), and the date of their initial DTI scan. All procedures were approved by the Emory University Institutional Animal Care and Use Committee.

Training Procedure

One member from each matched pair was randomly selected to be taught the DAID imitation game (IM) and the other served as a control (CO). Each IM/CO pair was trained concurrently (i.e., on the same days and during the same times of day) via positive reinforcement training. IM subjects learned to reproduce an experimenter's (EXP) action from a list of 23 DAID behaviors, whereas CO subjects were rewarded for producing basic husbandry behaviors in response to manual cues. Basic husbandry behaviors included presenting body parts, such as arms, legs, hands, feet, back, etc. All DAID actions are listed in Table 1. For lateralized DAID behaviors, IM subjects were trained to use the corresponding ipsilateral body part as the EXP (i.e., EXP's left = ape's right), as if they were looking in a mirror (Bekkering, Wohlschläger, & Gattis, 2000). IM and CO subjects each received 600’min of training (apart from one IM/CO pair, which received 602 and 589 min, respectively, due to experimenter error) and the number of days spent training ranged from 73 to 134 (M = 112.14, SD = 19.24). The number of days of training varied between subjects because of differences in training motivation from day to day, but there was no significant difference in the number of training days between the IM and CO groups, t(6) = −.15, p = .884. The number of training sessions ranged from 36 to 43 (M = 39, SD = 2.19), and the average session length ranged from 13.95 to 16.67 min (M = 15.39, SD = 0.88).

Table 1. 

DAID Behaviors Comprising Lists 1 and 2

List 1 List 2 
Protrude lips Protrude tongue 
Open mouth Lip smack 
Teeth chatter Puff cheeks 
Reach to side Reach across 
Foot raise Hand raise 
Pat head Pat belly 
Touch chin Touch nose 
Hand shake Wipe hands on floor 
Grasp wrist Wipe hands together 
Back of hand Fist 
Raised index Wave 
Touch elbow Touch armpit 
Touch knee Touch thigh 
Touch ear Touch back of head 
Both hands raise Both arms wide 
Clap Palm point 
Hands together front Hands together above head 
Peek-a-boo Wipe face 
Foot stomp Both feet raise 
Lay down 180-degree turn 
Shake head Stand up 
Cage bang Slap ground 
Hoo Extended grunt 
List 1 List 2 
Protrude lips Protrude tongue 
Open mouth Lip smack 
Teeth chatter Puff cheeks 
Reach to side Reach across 
Foot raise Hand raise 
Pat head Pat belly 
Touch chin Touch nose 
Hand shake Wipe hands on floor 
Grasp wrist Wipe hands together 
Back of hand Fist 
Raised index Wave 
Touch elbow Touch armpit 
Touch knee Touch thigh 
Touch ear Touch back of head 
Both hands raise Both arms wide 
Clap Palm point 
Hands together front Hands together above head 
Peek-a-boo Wipe face 
Foot stomp Both feet raise 
Lay down 180-degree turn 
Shake head Stand up 
Cage bang Slap ground 
Hoo Extended grunt 

Two different lists of 23 DAID behaviors were generated (Table 1). IM subjects were trained on one list of 23 actions and then tested for generalization in imitation performance on the remaining novel, 23 actions. Lists were composed of similar but distinct actions in an attempt to minimize differences in difficulty between lists. Training and test lists were counterbalanced, such that one male and one female were trained on List 1 and tested on List 2 and vice versa for the remaining two individuals.

Testing Procedure

Following training, all subjects were tested on their generalization in imitative abilities. During each test session, both trained and novel DAID actions were modeled for the subjects; each action was presented on three separate occasions for a total of 138 trials. To start a test session, subjects were engaged by prompting familiar, previously trained DAID (IM subjects) or husbandry (CO subjects) behaviors, followed by random presentations of novel actions. The novel modeled actions were presented by the experimenter for 10 sec, followed by the delivery of a small food reward, independent of their responses. In other words, no matter how the apes responded to the action modeled by the experimenter, they received a reward, thereby avoiding differential reinforcement of their behaviors. To keep subjects engaged, several familiar, previously trained behaviors (the exact number depended on the subject's motivation but ∼3) preceded each DAID test behavior. Testing sessions continued as long as the chimpanzees were engaged (i.e., remained proximal and attentive to EXP and produced the trained behaviors in response to cues) or until 46 test trials were administered (M = 4.5 sessions, SD = 1.2).

Test sessions were video-recorded (Canon HD Vixia HFS21) and later scored based on the following criteria: 3 = Subject used the corresponding ipsilateral body part to produce the demonstrated action. For example, EXP cage banged with right hand and the subject responded by cage banging with their left hand at least once within the 10 sec trial. 2 = Subject used a different or the corresponding contralateral body part to produce the demonstrated action or subject used the corresponding ipsilateral body part to produce a similar action. Using the above example (EXP cage bangs with their right hand), subjects would score a 2 if they (a) cage banged with their right hand or (b) waved their left hand (or any other action similar to cage bang). 1 = Subject used the corresponding ipsilateral body part to produce any action. Thus, if EXP cage banged with right hand, the subject could produce any action with their left hand and receive a score of 1. 0 = Subject did not use the corresponding body part and did not produce the demonstrated action. When subjects produced multiple actions within the 10 sec, the behavior with the highest score was recorded. To ensure that experimenter bias did not factor into scoring, 132 (12% of the total) test behaviors were re-coded by a second observer who was blind to both the subjects' training condition and the hypothesis. A Spearman rank order correlation between the two observers revealed the scoring of the chimpanzees' actions to be reliable (rho = .75, p < .05).

To compute each subject's overall performance, a cumulative imitation score was calculated. For IM subjects, 69 of the 138 behaviors presented during test sessions were from the familiar list that they were trained on and the remaining 69 were novel. However, for CO subjects, none of the 138 behaviors were familiar. Thus, IM subjects' imitation scores were calculated from only novel behaviors and because training occurred in CO/IM pairs, CO subjects' imitation scores were calculated based on the list that was novel to their IM counterpart to control for list difficulty. The three imitation scores for each of the 23 behaviors were summed (69 total scores) to derive a cumulative imitation score for each subject. Performance could vary from 0 to 207 (3 trials × 23 actions × a score of 3). Because of EXP error, one CO subject only received two tests for one of the behaviors (68 total scores); thus, their highest score for that behavior was used again, as a conservative third score.

Scanning Protocol

In vivo MRI and DTI scans were obtained at the same time that the chimpanzees were participating in their annual physical examinations, which was coordinated with the end of their training. Subjects were first immobilized by ketamine (10 mg/kg) or telazol (3–5 mg/kg) and subsequently anaesthetized with propofol (40–60 mg/(kg/hr)) following standard procedures at the YNPRC. Subjects were then transported to the YNPRC MRI facility and were placed in the scanner chamber in a supine position with their head fitted inside the human-head coil. The subjects remained anaesthetized for the duration of the scans as well as the time needed to transport them between their home cage and the imaging facility (total time ∼ 1.5 hr). After scanning was completed, the apes were returned to their home cage and allowed to fully recover from the anesthesia before being reunited with their group members. Within pairs of subjects, the time between pre- and post-DTI scans ranged from 0.02 to 0.50 years (M = 0.22, SD = 0.23). Time between final training day and post-DTI scan ranged from 6 to 18 days (M = 11.57, SD = 4.49); however, there was no difference between IM and CO apes, t (6) = −2.93, p = .06.

Subjects were imaged using a 3.0 T Siemens Trio scanner (Siemens Medical Solutions USA, Inc., Malvern, PA). T1-weighted images were collected using a three-dimensional gradient-echo sequence (pulse repetition = 2300 msec, echo time = 4.4 msec, number of signals averaged = 3, matrix size = 320 × 320). Scanning parameters were slightly different for the first two DTIs (one CO and one IM) than for the remaining 14. For all scans, two whole-brain diffusion-weighted data sets, with a single shot EPI sequence and a b value of 1000 sec/mm2 with 64 (Scans 1–2 = 60) diffusion directions, along with an additional image without diffusion weighting (b value = 0 sec/mm2) were acquired. Acquisition occurred transaxially: for Scans 1–2 FOV = 230 and resolution = 1.8 × 1.8’× 1.8 mm for 60 slices; for Scans 3–16 FOV = 243 and resolution = 1.9 × 1.9 × 1.9 mm for 42 slices. Diffusion-weighted data with phase-encoding directions of opposite polarity were averaged (Scans 1–2 = 10 averages; Scans 2–6 = 1 average) to correct for susceptibility to distortion. Preprocessing was performed using The Oxford Center for Functional Magnetic Resonance Imaging (FMRIB) software, FSL (www.fmrib.ox.ac.uk/fsl) and consisted of (1) reorientation, (2) removal of nonbrain tissue using the Brain Extraction Tool, (3) head motion correction, and (4) eddy current distortion correction (FDT toolbox). DTIFIT was used to fit diffusion tensors at each voxel to create fractional anisotropy (FA) maps. Radial diffusivity (RD) maps were then calculated from the DTIFIT output by summing the L2 and L3 volumes and dividing by 2. To assess probabilistic tractography, diffusion gradient information was reconstructed using FSL's BEDPOSTX tool within the FDT toolkit (Behrens et al., 2007). All image preprocessing followed standard procedures outlined in the FDT userguide.

ROIs

To assess changes within and between frontoparietotemporal regions, bilateral ROIs were manually traced onto each subject's previously collected T1-weighted MRI scans (Autrey et al., 2014). The landmarks used to identify each of the three ROIs are defined below and shown in Figure 1.

Figure 1. 

(A) ROIs for the hypothesized chimpanzee mirror system composed of IFG, IPL, and STS regions and (B) ROIs for the geniculostriate control tract composed of an occipital slice and the optic chiasm.

Figure 1. 

(A) ROIs for the hypothesized chimpanzee mirror system composed of IFG, IPL, and STS regions and (B) ROIs for the geniculostriate control tract composed of an occipital slice and the optic chiasm.

Inferior Frontal Gyrus

In the axial plane, the ROI was defined as the area between the fronto-orbital and inferior precentral sulci (PCI) with the medial boundary being a straight line between the medial edges of the two sulci. Following axial tracing, the image was returned to the sagittal plane and the first lateral slice where the insula was no longer visible was located. The ROI was extended from the bottom-left corner of this slice either along PCI if it was still apparent or straight down if it was not. This was repeated for all remaining slices, moving laterally.

Inferior Parietal Lobe

First, the image was placed in the sagittal plane, where the most medial slice in which the insula was not visible was identified. A line was then drawn from the most anterior extension of the postcentral sulcus (PoC) straight down to the lateral sulcus (Lt). This served as the anterior boundary. Next, the dorsal boundary was marked as the point that the PoC was no longer parallel to the Lt. Finally, a diagonal line was drawn from this dorsal boundary to the Lt, which served as the posterior boundary. The image was then rotated into the axial plane, and the area between the PoC and Lt, within the predefined bounds, was captured.

STS

First, the image was placed in the sagittal plane, where the most medial slice in which the insula is not visible was identified. The gray matter between the superior temporal and the medial-temporal gyri was traced. The dorsal boundary was marked at the intersection with the inferior parietal sulcus. Moving laterally, the area between the superior temporal and medial-temporal gyri was captured in each slice. Next, the image was rotated into the coronal plane where the extreme medial and lateral extensions of the STS were captured for all slices.

FA and RD Methods

Within the putative mirror system, changes in FA, which indicates how uniformly directional diffusivity is within a given voxel as a proxy for tract integrity, and RD, which indicates myelination by measuring the rate of diffusivity in the perpendicular direction, were compared between training conditions. Processed FA and RD maps for both pre- and postscans were linearly registered to subjects' previously collected, T1-weighted MRI scans. Following this registration, subject-specific frontoparietotemporal ROIs and pre/post FA and RD maps were in the same stereotaxic space. Next, ROIs for each hemisphere were placed on the registered FA and RD volume, and the average value within the ROI was calculated. Variation in signal-to-noise ratios between scans was adjusted by dividing the mean FA and mean RD within each ROI by the mean FA and RD, respectively, within that hemisphere or by the mean whole-brain FA and RD, respectively, for bilateral analyses, for each scan. Finally, the pre FA and RD values were subtracted from post FA and RD values to reflect measures of change in white matter integrity within each ROI within the frontoparietotemporal regions for each subject.

Probabalistic Tractography Methods

To assess potential changes in mirror system white matter connectivity, we used FSL's software package for probabilistic tractography, PROBTRACKx (Behrens et al., 2007). First, registration matrices were created and used to place diffusion gradient information for each scan (generated from BEDPOSTx) into the same stereotaxic space as subjects' T1-weighted MRI scan. Probabalistic tractrography was then used to assess the connectivity distributions between ROIs. To increase the likelihood that streamlines were generated within ROIs and not underlying white matter tracts passing through the ROI, seed ROIs were masked to only include gray matter. We chose to use networks mode tractography, which includes bidirectional streamlines passing through all ROIs, and a midline exclusion mask to prevent them crossing into the contralateral hemisphere. Thus, all connectivity maps were intrahemispheric. To account for differences in brain size due to diffusion data being in subjects' native space (rather than template space), we incorporated distance correction into the tractography algorithm. All other default settings were used (5000 samples were generated from each seed voxel, 0.2 curvature threshold, 0.5’mm step length, 2000 maximum number of steps, loopcheck enabled, and waypoints were applied independently to both directions). In this manner, connectivity distribution maps were generated for (1) IFG-IPL, (2) IFG-STS, and (3) IPL-STS. To control for differences in scan quality, connectivity maps were divided by the waytotal (the total number of streamlines within a connectivity map) of a control tract—the geniculostriate—for each hemisphere. The geniculostriate tract was generated by seeding coronal sections of the optic chiasm and occipital white matter (see Figure 1). From these normalized connectivity maps, the mean voxel intensity (a measure of how many streamlines pass through a given voxel) was calculated, which reflects “tract strength.” In addition, the total number of voxels comprising the tract was also calculated, which was defined as “tract volume.” Tract volume values were also normalized by dividing by the geniculostriate waytotal.

We chose not to apply thresholding to connectivity maps for two reasons. First, thresholding is typically used to exclude erroneous streamlines from analysis; however, our inclusion of the control group already addresses this issue (i.e., error should be equally distributed across IM and CO subjects). Second, thresholding would limit analyses to only the most established tracts, which may be less likely to change—due to ceiling effects—following training. In other words, training-induced increases in connectivity may occur less readily in voxels already containing a large proportion of the streamlines.

Data Analysis

We analyzed the data two ways. First, we identified mean FA, mean RD, tract strength, and tract volume when summed across the two hemispheres for each ROI/tract to identify bilateral frontoparietotemporal changes. Second, we tested for changes in lateralization of mean FA, mean RD, tract strength, and tract volume to gain an understanding of any asymmetrical frontoparietotemporal changes. To assess the magnitude and direction of lateralized changes following imitation training, asymmetry quotients (AQ) were calculated following the formula [AQ = (RL) / ((R + L) × .5)] where R and L represented the normalized mean FA and RD and mean strength and volume within each tract for the right and left hemispheres. Negative values indicated leftward asymmetries, whereas positive values indicated rightward biases. Next, changes in AQ scores (ΔAQ) were calculated by subtracting each subject's prescan AQ score from the postscan AQ score, of which the absolute value indicated the magnitude of the change but not the direction. We then differentiated between leftward and rightward changes by setting these magnitude values to negative and positive, respectively. This was done for IFG, IPL, and STS ROIs and IFG-IPL, IFG-STS, and IPL-STS tracts.

Figure 2. 

Mean (and SE) changes in AQ for FA within mirror system ROIs following training in IM subjects (solid gray) and CO subjects (checker). Positive values indicate increases in the right hemisphere as compared with the left, whereas negative values indicate increases in the left hemisphere as compared with the right.

Figure 2. 

Mean (and SE) changes in AQ for FA within mirror system ROIs following training in IM subjects (solid gray) and CO subjects (checker). Positive values indicate increases in the right hemisphere as compared with the left, whereas negative values indicate increases in the left hemisphere as compared with the right.

RESULTS

Behavioral Analysis

To determine if DAID imitation training generalized to imitation of novel behaviors, DAID scores were compared between training conditions. IM subjects had significantly higher mean novel imitation scores (M = 100.5, SD = 21.49) as compared with CO subjects (M = 52.50, SD = 9.75), t(6) = 4.069, p = .007. The results were consistent across all four IM/CO pairs, with the IM subjects performing significantly better than their CO match (see Table 2).

Table 2. 

Novel DAID Behavior Test Scores for Each IM/CO Subject Pair

IM Sum CO Sum 
Carl 84 Fritz 59 
Jacqueline 100 Cissie 48 
Faye 87 Evelyne 41 
Gelb 131 David 62 
 
Average 100.5  52.5 
SE 10.74  4.87 
IM Sum CO Sum 
Carl 84 Fritz 59 
Jacqueline 100 Cissie 48 
Faye 87 Evelyne 41 
Gelb 131 David 62 
 
Average 100.5  52.5 
SE 10.74  4.87 

FA and RD

As a measure of overall change in frontoparietotemporal white matter integrity, bilateral changes in mean FA and mean RD were calculated. Left and right hemisphere values were summed, and prescan values were subtracted from postscan values, for each ROI. Mixed-model repeated-measures ANOVAs revealed no significant effects of training condition for overall frontoparietotemporal FA or RD values.

Next, lateralized effects of training condition on frontoparietotemporal white matter integrity were assessed. A mixed-model repeated-measures ANOVA, with ΔAQ as the repeated-measure and Training condition as the between subjects variable, revealed a significant between-subject effect of Training condition on mean FA, F(1, 6) = 6.12, p = .048 (Figure 2). IM subjects showed leftward increases in FA for all frontoparietotemporal ROIs. There were no significant changes in ΔAQ for mean RD. Means and standard deviations for all FA and RD measures are presented in Table 3.

Figure 3. 

Mean (and SE) changes in AQ for MNS tract strength following imitation training in IM subjects (solid gray) and CO subjects (checker). Positive values indicate increases in the right hemisphere as compared with the left, whereas negative values indicate increases in the left hemisphere as compared with the right.

Figure 3. 

Mean (and SE) changes in AQ for MNS tract strength following imitation training in IM subjects (solid gray) and CO subjects (checker). Positive values indicate increases in the right hemisphere as compared with the left, whereas negative values indicate increases in the left hemisphere as compared with the right.

Table 3. 

Means and Standard Deviations (in Parentheses) for the Differences in FA and RD between Pre- and Postscans

 IFG IPL STS 
CO IM CO IM CO IM 
FA total 0.001 −0.061 −0.064 −0.012 −0.026 0.068 
(0.163) (0.071) (0.062) (0.157) (0.245) (0.214) 
RD total −0.041 0.027 0.042 −0.003 −0.004 −0.040 
(0.065) (0.082) (0.057) (0.089) (0.164) (0.132) 
FA AQ 0.004 −0.036 0.072 −0.052 0.005 −0.079 
(0.038) (0.066) (0.048) (0.096) (0.074) (0.168) 
RD AQ 0.009 −0.001 −0.015 0.011 0.006 0.018 
(0.030) (0.020) (0.022) (0.044) (0.015) (0.070) 
 IFG IPL STS 
CO IM CO IM CO IM 
FA total 0.001 −0.061 −0.064 −0.012 −0.026 0.068 
(0.163) (0.071) (0.062) (0.157) (0.245) (0.214) 
RD total −0.041 0.027 0.042 −0.003 −0.004 −0.040 
(0.065) (0.082) (0.057) (0.089) (0.164) (0.132) 
FA AQ 0.004 −0.036 0.072 −0.052 0.005 −0.079 
(0.038) (0.066) (0.048) (0.096) (0.074) (0.168) 
RD AQ 0.009 −0.001 −0.015 0.011 0.006 0.018 
(0.030) (0.020) (0.022) (0.044) (0.015) (0.070) 

Tractography

To assess overall changes in white matter connectivity between frontoparietotemporal ROIs, bilateral tract strength and volume measures were calculated. Values from left and right hemispheres were summed, and prescan values were subtracted from postscan values for each tract. Mixed-model repeated-measures ANOVAs revealed no significant changes in overall frontoparietotemporal connectivity.

Next, lateralized effects of training condition on white matter connectivity were determined. Changes in AQ for mean tract strength and volume were assessed using mixed-model repeated-measures ANOVAs, with ΔAQ as the repeated-measure and Training condition as the between-group factor. A significant between-subject effect of Training condition was found for mean tract strength, F(1, 6) = 6.910, p = .039 (Figure 3). Similar to FA within ROIs, IM subjects showed leftward increases in mean tract strength between all frontoparietotemporal ROIs. No significant changes were found for tract volume ΔAQ. Means and standard deviations for all tract strength and volume measures are presented in Table 4.

Figure 4. 

The average increases (note that this does not depict the decreases in connectivity that are accounted for in the AQ measure) in right (red) and left (green) tract intensity between pre- and postscans in CO and IM subjects' probabalistic tractography maps. Bilateralal increases in connectivity were apparent in CO subjects' IFG-IPL tract and rightward increases were seen in IFG-STS and IPL-STS tracts. IM subjects, however, exhibited greater leftward increases across IFG-IPL, IFG-STS, and IPL-STS tracts.

Figure 4. 

The average increases (note that this does not depict the decreases in connectivity that are accounted for in the AQ measure) in right (red) and left (green) tract intensity between pre- and postscans in CO and IM subjects' probabalistic tractography maps. Bilateralal increases in connectivity were apparent in CO subjects' IFG-IPL tract and rightward increases were seen in IFG-STS and IPL-STS tracts. IM subjects, however, exhibited greater leftward increases across IFG-IPL, IFG-STS, and IPL-STS tracts.

Table 4. 

Means and Standard Deviations (in Parentheses) for the Differences in Tract Strength and Volume between Pre- and Postscans

 IFG-IPL IFG-STS IPL-STS 
CO IM CO IM CO IM 
Strength total 0.242 0.096 0.197 0.016 0.036 0.140 
(0.307) (0.277) (0.264) (0.198) (0.297) (0.308) 
Volume total −3.72 −7.54 −3.83 −6.18 −4.27 −4.98 
(4.00) (6.14) (4.85) (3.50) (2.61) (3.33) 
Strength AQ 0.366 −0.990 0.258 −1.00 0.565 −0.844 
(0.329) (0.575) (0.623) (1.14) (0.882) (0.946) 
Volume AQ −0.371 0.022 −0.474 0.052 −0.212 0.127 
(0.425) (0.533) (0.390) (0.764) (0.137) (0.418) 
 IFG-IPL IFG-STS IPL-STS 
CO IM CO IM CO IM 
Strength total 0.242 0.096 0.197 0.016 0.036 0.140 
(0.307) (0.277) (0.264) (0.198) (0.297) (0.308) 
Volume total −3.72 −7.54 −3.83 −6.18 −4.27 −4.98 
(4.00) (6.14) (4.85) (3.50) (2.61) (3.33) 
Strength AQ 0.366 −0.990 0.258 −1.00 0.565 −0.844 
(0.329) (0.575) (0.623) (1.14) (0.882) (0.946) 
Volume AQ −0.371 0.022 −0.474 0.052 −0.212 0.127 
(0.425) (0.533) (0.390) (0.764) (0.137) (0.418) 

DISCUSSION

The current study reports two main findings. First, adult chimpanzees that were DAID trained were better able to copy novel behaviors than nonimitation trained controls. This generalization from trained imitative behaviors to the imitation of novel actions has been reported in juvenile chimpanzees (Custance et al., 1995). However, this is the first instance in which such transfer occurred in adults, illustrating continued behavioral plasticity for DAID imitation learning past the period of juvenile development in chimpanzees. Second, this study is the first to show imitation related neural plasticity in nonhuman apes. Specifically, following DAID imitation training, significant leftward increases were found in the white matter integrity of frontoparietotemporal regions that make up the putative chimpanzee mirror system (Figure 4).

Our findings provide further evidence that chimpanzees are capable of imitative behaviors (see Whiten, 2017, for a review), which may be honed through DAID training. We suggest that DAID practice strengthened IM subjects' existing frontoparietotemporal imitation system, the presence of which has been indicated by other recent findings showing that juvenile chimpanzees exhibit seemingly automatic motor mimicry while learning nut-cracking behavior (Fuhrmann, Ravignani, Marshall-Pescini, & Whiten, 2014). To clarify, control subjects' decreased propensity toward imitative behaviors during testing should not be taken as evidence that they did not know how to imitate or that imitation itself was trained in IM subjects. DAID training simply provided IM subjects with an environment in which imitation was rewarded and subsequently practiced. Thus, during testing, CO subjects were playing a game for which they did not know the rules.

DAID training and participation induced left lateralized increases in frontoparietotemporal white matter integrity in chimpanzees. These changes were found in mean FA (a measure of tract integrity) within frontoparietotemporal ROIs and in mean tract strength (the number of identified streamlines passing through any given voxel) connecting those ROIs. It is likely that this reflects increased myelination of existing pathways such that they became strong enough for inclusion by the probabilistic tractography algorithm. Furthermore, the significant leftward increase in FA within the frontoparietotemporal ROIs is consistent with this interpretation. Although high FA/RD ratios have been used to identify increases in myelination (Li, Legault, & Litcofsky, 2014), this study found no significant changes in RD. This is likely because we were limited to measuring FA and RD within predominantly gray matter ROIs and not in the white matter connections between the ROIs where the majority of myelination increases might occur.

Leftward dominance has also been found in the human frontoparietotemporal mirror system. Patients with lesions show more imitative deficits when the damage is on the left side (Goldenberg, 1996). Specifically, damage to the left IPL impairs patient's ability to conceptualize the action to be imitated (Halsband et al., 2001; Goldenberg, 1999). In a pivotal study, bilateral activation was seen following finger movement imitation in controls but only left activation was seen in split-brain patients, indicating that bilateral neural involvement in imitation may be driven by callosal connections from left to right hemispheres (Fecteau, Lassonde, & Théoret, 2005). Thus, the current study's findings implicating left dominance within a frontoparietotemporal imitation system in chimpanzees further supports the notion of homologous neural underpinnings of imitation in human and nonhuman apes.

There are three primary limitations of this study. First, by using ROIs we excluded large portions of neural architecture, which might have experienced DAID training-related changes, from our analyses. However, more inclusive techniques (e.g., Tract-Based Spatial Statistics) require much greater sample sizes and were therefore not feasible under the current methodology. Second, ideally the baseline initial scans would have occurred immediately before training; however, to limit the stress placed on the animals, we opted to use previously collected DTIs. This choice necessitated the inclusion of a control group matched for the time between pre- and postscans, such that natural changes with time would be similar across conditions. Thus, bilateral positive and negative changes could be reasonably expected in both IM and CO subjects. We suggest that the almost entirely positive, unilateral changes within the left mirror system of IM subjects is even more striking, given the bidirectional changes that likely occurred before training. Note, all lateralized trained actions (imitative and control) were presented equally for left and right sides. Second, we chose body part presentation as the control training procedure because, like imitation training, it involves full body, bilateral movements and a high degree of experimenter–subject interaction. Notably, some of the cues for body parts are similar to the actions themselves (ex. present hand cue is EXP's hand, palm down), making this control extremely conservative, as some of the control behavior cues and responses border on imitative. Although we did not test CO subjects' body part presentation abilities following training, subjectively they appeared to improve. Of course, we are not advocating that frontoparietotemporal regions are exclusively involved in imitative behaviors; thus, it is plausible that some of CO subjects' changes in these regions were a function of their own training.

The observed left-biased mirror system related to imitation in chimpanzees has some potential implications for the evolution of language. The neural underpinnings of speech are typically left-lateralized and involve Broca's area, a region morphologically and cytoarchitectonically homologous to the chimpanzee IFG (Keller, Roberts, & Hopkins, 2009; Schenker et al., 2008; Sherwood, Broadfield, Holloway, Gannon, & Hof, 2003). Furthermore, in chimpanzees, the left IFG is involved in gestural and vocal intentional communication (Taglialatela, Russell, Schaeffer, & Hopkins, 2008). When we consider the extent to which imitation plays a role in the development of language and other social skills, it follows that similar neural regions might underlie these abilities. Indeed, we have previously found that chimpanzees that perform better on an imitation recognition task also perform significantly better on measures of social cognition and sociocommunicative competencies (Pope et al., 2015). Thus, the current study indicates that a left-dominant imitation system might have predated the Pan–Homo divergence, thereby providing indirect support for theories suggesting that language might have been built upon or in conjunction with the emergence of increasingly sophisticated imitation recognition and learning skills.

Acknowledgments

This research was supported by NIH grants NS-42867, NS-73134, HD-60563 to W. D. H. and DC-011005 to J. P. T. In addition, S. M. P. is funded by Georgia State University's Second Century Initiative Primate Social Cognition, Evolution, and Behavior fellowship and the Kenneth W. and Georganne F. Honeycutt Fellowship. We would also like to thank Kendall Davidek for her time and efforts in verifying interrater reliability. American Psychological Association and Institute of Medicine guidelines for the treatment of animals were followed during all aspects of this study.

Reprint requests should be sent to William D. Hopkins, Neuroscience Institute and Language Research Center, Georgia State University, P.O. Box 5030, Atlanta, GA 30302-5030, or via e-mail: whopkins4@gsu.edu or whopkin@emory.edu.

REFERENCES

Allison
,
T.
,
Puce
,
A.
, &
McCarthy
,
G.
(
2000
).
Social perception from visual cues: Role of the STS region
.
Trends in Cognitive Sciences
,
4
,
267
278
.
Asendorpf
,
J. B.
,
Warkentin
,
V.
, &
Baudonnière
,
P.-M.
(
1996
).
Self-awareness and other-awareness II: Mirror self-recognition, social contingency awareness, and synchronic imitation
.
Developmental Psychology
,
32
,
313
321
.
Autrey
,
M. M.
,
Reamer
,
L. A.
,
Mareno
,
M. C.
,
Sherwood
,
C. C.
,
Herndon
,
J. G.
,
Preuss
,
T.
, et al
(
2014
).
Age-related effects in the neocortical organization of chimpanzees: Gray and white matter volume, cortical thickness, and gyrification
.
Neuroimage
,
101
,
59
67
.
Bard
,
K. A.
(
2007
).
Neonatal imitation in chimpanzees (Pan troglodytes) tested with two paradigms
.
Animal Cognition
,
10
,
233
242
.
Bekkering
,
H.
,
Wohlschläger
,
A.
, &
Gattis
,
M.
(
2000
).
Imitation of gestures in children is goal-directed
.
Quarterly Journal of Experimental Psychology
,
53A
,
153
164
.
Behrens
,
T. E.
,
Berg
,
H. J.
,
Jbabdi
,
S.
,
Rushworth
,
M. F.
, &
Woolrich
,
M. W.
(
2007
).
Probabilistic diffusion tractography with multiple fibre orientations: What can we gain?
Neuroimage
,
34
,
144
155
.
Buttelmann
,
D.
,
Carpenter
,
M.
,
Call
,
J.
, &
Tomasello
,
M.
(
2007
).
Enculturated chimpanzees imitate rationally
.
Developmental Science
,
10
,
F31
F38
.
Buttelmann
,
D.
,
Carpenter
,
M.
,
Call
,
J.
, &
Tomasello
,
M.
(
2013
).
Chimpanzees, Pan troglodytes, recognize successful actions, but fail to imitate them
.
Animal Behaviour
,
86
,
755
761
.
Call
,
J.
(
2001
).
Body imitation in an enculturated orangutan (Pongo pygmaeus)
.
Cybernetics and Systems
,
32
,
97
119
.
Call
,
J.
,
Carpenter
,
M.
, &
Tomasello
,
M.
(
2005
).
Copying results and copying actions in the process of social learning: Chimpanzees (Pan troglodytes) and human children (Homo sapiens)
.
Animal Cognition
,
8
,
151
163
.
Carpenter
,
M.
, &
Call
,
J.
(
2009
).
Comparing the imitative skills of children and nonhuman apes
.
Revue de Primatologie
,
1
.
doi:10.4000/primatologie.263
.
Carpenter
,
M.
,
Tomasello
,
M.
, &
Savagerumbaugh
,
S.
(
1995
).
Joint-attention and imitative learning in children, chimpanzees, and enculturated chimpanzees
.
Social Development
,
4
,
217
237
.
Carr
,
L.
,
Iacoboni
,
M.
,
Dubeau
,
M.-C.
,
Mazziotta
,
J. C.
, &
Lenzi
,
G. L.
(
2003
).
Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas
.
Proceedings of the National Academy of Sciences, U.S.A.
,
100
,
5497
5502
.
Charman
,
T.
,
Swettenham
,
J.
,
Baron-Cohen
,
S.
,
Cox
,
A.
,
Baird
,
G.
, &
Drew
,
A.
(
1997
).
Infants with autism: An investigation of empathy, pretend play, joint attention, and imitation
.
Developmental Psychology
,
33
,
781
789
.
Corballis
,
M. C.
(
2010
).
Mirror neurons and the evolution of language
.
Brain and Language
,
112
,
25
35
.
Custance
,
D. M.
,
Whiten
,
A.
, &
Bard
,
K. A.
(
1995
).
Can young chimpanzees (Pan troglodytes) imitate arbitrary actions? Hayes and Hayes (1952) revisited
.
Behaviour
,
132
,
837
859
.
di Pellegrino
,
G.
,
Fadiga
,
L.
,
Fogassi
,
L.
,
Gallese
,
V.
, &
Rizzolatti
,
G.
(
1992
).
Understanding motor events: A neurophysiological study
.
Experimental Brain Research
,
91
,
176
180
.
Fabbri-Destro
,
M.
, &
Rizzolatti
,
G.
(
2008
).
Mirror neurons and mirror systems in monkeys and humans
.
Physiology
,
23
,
171
179
.
Fecteau
,
S.
,
Lassonde
,
M.
, &
Théoret
,
H.
(
2005
).
Modulation of motor cortex excitability during action observation in disconnected hemispheres
.
NeuroReport
,
16
,
1591
1594
.
Fragaszy
,
D. M.
,
Deputte
,
B.
,
Cooper
,
E. J.
,
Colbert-White
,
E. N.
, &
Hemery
,
C.
(
2011
).
When and how well can human-socialized capuchins match actions demonstrated by a familiar human?
American Journal of Primatology
,
73
,
643
654
.
Fuhrmann
,
D.
,
Ravignani
,
A.
,
Marshall Pescini
,
S.
, &
Whiten
,
A.
(
2014
).
Synchrony and motor mimicking in chimpanzee observational learning
.
Scienctific Reports
,
4
,
5283
.
Galef
,
B. G.
(
2012
).
Social learning and traditions in animals: Evidence, definitions, and relationship to human culture
.
Wiley Interdisciplinary Reviews: Cognitive Science
,
3
,
581
592
.
Gallese
,
V.
,
Fadiga
,
L.
,
Fogassi
,
L.
, &
Rizzolatti
,
G.
(
1996
).
Action recognition in the premotor cortex
.
Brain
,
119
,
593
609
.
Gallese
,
V.
,
Fadiga
,
L.
,
Fogassi
,
L.
, &
Rizzolatti
,
G.
(
2002
).
Action representation and the inferior parietal lobule
. In
W.
Prinz
&
B.
Hommel
(Eds.),
Common mechanisms in perception and action: Attention and performance
(pp.
247
266
).
Oxford
:
Oxford University Press
.
Goldenberg
,
G.
(
1996
).
Defective imitation of gestures in patients with damage in the left or right hemispheres
.
Journal of Neurology, Neurosurgery, and Psychiatry
,
61
,
176
180
.
Goldenberg
,
G.
(
1999
).
Matching and imitation of hand and finger postures in patients with damage in the left or right hemispheres
.
Neuropsychologia
,
37
,
559
566
.
Halsband
,
U.
,
Schmitt
,
J.
,
Weyers
,
M.
,
Binkofski
,
F.
,
Grützner
,
G.
, &
Freund
,
H. J.
(
2001
).
Recognition and imitation of pantomimed motor acts after unilateral parietal and premotor lesions: A perspective on apraxia
.
Neuropsychologia
,
39
,
200
216
.
Haun
,
D. B.
, &
Call
,
J.
(
2008
).
Imitation recognition in great apes
.
Current Biology
,
18
,
R288
R290
.
Hayes
,
K. J.
, &
Hayes
,
C.
(
1952
).
Imitation in a home-raised chimpanzee
.
Journal of Comparative and Physiological Psychology
,
45
,
450
459
.
Hecht
,
E. E.
,
Gutman
,
D. A.
,
Preuss
,
T. M.
,
Sanchez
,
M. M.
,
Parr
,
L. A.
, &
Rilling
,
J. K.
(
2013
).
Process versus product in social learning: Comparative diffusion tensor imaging of neural systems for action execution-observation matching in macaques, chimpanzees, and humans
.
Cerebral Cortex
,
23
,
1014
1024
.
Heyes
,
C. M.
(
1993
).
Imitation, culture and cognition
.
Animal Behaviour
,
46
,
999
1010
.
Hickok
,
G.
(
2009
).
Eight problems for the mirror neuron theory of action understanding in monkeys and humans
.
Journal of Cognitive Neuroscience
,
21
,
1229
1243
.
Horner
,
V.
, &
Whiten
,
A.
(
2005
).
Causal knowledge and imitation/emulation switching in chimpanzees (Pan troglodytes) and children (Homo sapiens)
.
Animal Cognition
,
8
,
164
181
.
Hyde
,
K. L.
,
Lerch
,
J.
,
Norton
,
A.
,
Forgeard
,
M.
,
Winner
,
E.
,
Evans
,
A. C.
, et al
(
2009
).
Musical training shapes structural brain development
.
Journal of Neuroscience
,
29
,
3019
3025
.
Iacoboni
,
M.
(
2009
).
Imitation, empathy, and mirror neurons
.
Annual Review of Psychology
,
60
,
653
670
.
Iacoboni
,
M.
, &
Wilson
,
S. M.
(
2006
).
Beyond a single area: Motor control and language within a neural architecture encompassing Broca's area
.
Cortex
,
42
,
503
506
.
Iacoboni
,
M.
,
Woods
,
R. P.
,
Brass
,
M.
,
Bekkering
,
H.
,
Mazziotta
,
J. C.
, &
Rizzolatti
,
G.
(
1999
).
Cortical mechanisms of human imitation
.
Science
,
286
,
2526
2528
.
Keller
,
S. S.
,
Roberts
,
N.
, &
Hopkins
,
W.
(
2009
).
A comparative magnetic resonance imaging study of the anatomy, variability, and asymmetry of Broca's area in the human and chimpanzee brain
.
Journal of Neuroscience
,
29
,
14607
14616
.
Koski
,
L.
,
Wohlschläger
,
A.
,
Bekkering
,
H.
,
Woods
,
R. P.
,
Dubeau
,
M. C.
,
Mazziotta
,
J. C.
, et al
(
2002
).
Modulation of motor and premotor activity during imitation of target-directed actions
.
Cerebral Cortex
,
12
,
847
855
.
Li
,
P.
,
Legault
,
J.
, &
Litcofsky
,
K. A.
(
2014
).
Neuroplasticity as a function of second language learning: Anatomical changes in the human brain
.
Cortex
,
58
,
301
324
.
Meltzoff
,
A. N.
(
1988
).
The human infant as Homo imitans
. In
T. R. G.
Zentall
&
B. G.
Galef
(Eds.),
Social learning: Psychological and biological perspectives
(pp.
319
341
).
Hillsdale, NJ
:
Erlbaum
.
Meltzoff
,
A. N.
(
1990
).
Foundations for developing a concept of self: The role of imitation in relating self to other and the value of social mirroring, social modeling, and self practice in infancy
. In
D.
Cicchetti
&
M.
Beeghly
(Eds.),
The self in transition: Infancy to childhood
(pp.
139
164
).
Chicago
:
University of Chicago Press
.
Meltzoff
,
A. N.
, &
Moore
,
M. K.
(
1977
).
Imitation of facial and manual gestures by human neonates
.
Science
,
198
,
75
78
.
Mitchell
,
R. W.
, &
Anderson
,
J. R.
(
1993
).
Discrimination learning of scratching, but failure to obtain imitation and self-recognition in a long-tailed macaque
.
Primates
,
34
,
301
309
.
Myowa-Yamakoshi
,
M.
, &
Matsuzawa
,
T.
(
2000
).
Imitation in intentional manipulatory actions in chimpanzees (Pan troglodytes)
.
Journal of Comparative Psychology
,
114
,
381
391
.
Myowa-Yamakoshi
,
M.
,
Tomonaga
,
M.
,
Tanaka
,
M.
, &
Matsuzawa
,
T.
(
2004
).
Imitation in neonatal chimpanzees (Pan troglodytes)
.
Developmental Science
,
7
,
437
442
.
Nadel
,
J.
(
2002
).
Imitation and imitation recognition: Functional use in preverbal infants and nonverbal children with autism
. In
A. N.
Meltzoff
&
W.
Prinz
(Eds.),
The imitative mind: Development, evolution, and brain bases
(pp.
42
62
).
Cambridge, U.K.
:
Cambridge University Press
.
Nielsen
,
M.
, &
Dissanayake
,
C.
(
2004
).
Pretend play, mirror self-recognition and imitation: A longitudinal investigation through the second year
.
Infant Behavior & Development
,
27
,
342
365
.
Paukner
,
A.
,
Anderson
,
J. R.
,
Borelli
,
E.
,
Visalberghi
,
E.
, &
Ferrari
,
P. F.
(
2005
).
Macaques (Macaca nemestrina) recognize when they are being imitated
.
Biology Letters
,
1
,
219
222
.
Paukner
,
A.
,
Pedersen
,
E. J.
, &
Simpson
,
E. A.
(
2017
).
Testing the arousal hypothesis of neonatal imitation in infant rhesus macaques
.
PLoS One
,
12
,
e0178864
.
Paukner
,
A.
,
Simpson
,
E. A.
,
Ferrari
,
P. F.
,
Mrozek
,
T.
, &
Suomi
,
S. J.
(
2014
).
Neonatal imitation predicts how infants engage with faces
.
Developmental Science
,
17
,
833
840
.
Paukner
,
A.
,
Suomi
,
S. J.
,
Visalberghi
,
E.
, &
Ferrari
,
P. F.
(
2009
).
Capuchin monkeys display affiliation toward humans who imitate them
.
Science
,
325
,
880
883
.
Perrett
,
D. I.
,
Harries
,
M. H.
,
Mistlin
,
A. J.
,
Hietanen
,
J. K.
,
Benson
,
P. J.
,
Bevan
,
R.
, et al
(
1990
).
Social signals analyzed at the single cell level: Someone is looking at me, something touched me, something moved!
International Journal of Comparative Psychology
,
4
,
25
55
.
Pfeifer
,
J. H.
,
Iacoboni
,
M.
,
Mazziotta
,
J. C.
, &
Dapretto
,
M.
(
2008
).
Mirroring others' emotions relates to empathy and interpersonal competence in children
.
Neuroimage
,
39
,
2076
2085
.
Pope
,
S. M.
,
Russell
,
J. L.
, &
Hopkins
,
W. D.
(
2015
).
The association between imitation recognition and socio-communicative competencies in chimpanzees (Pan troglodytes)
.
Frontiers in Psychology
,
6
,
188
.
Rizzolatti
,
G.
, &
Craighero
,
L.
(
2004
).
The mirror-neuron system
.
Annual Review of Neuroscience
,
27
,
169
192
.
Rizzolatti
,
G.
, &
Fogassi
,
L.
(
2014
).
The mirror mechanism: Recent findings and perspectives
.
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
,
369
,
20130420
.
Rizzolatti
,
G.
,
Fogassi
,
L.
, &
Gallese
,
V.
(
2002
).
Motor and cognitive functions of the ventral premotor cortex
.
Current Opinion in Neurobiology
,
12
,
149
154
.
Schenker
,
N. M.
,
Buxhoeveden
,
D. P.
,
Blackmon
,
W. L.
,
Amunts
,
K.
,
Zilles
,
K.
, &
Semendeferi
,
K.
(
2008
).
A comparative quantitative analysis of cytoarchitecture and minicolumnar organization in Broca's area in humans and great apes
.
Journal of Comparative Neurology
,
510
,
117
128
.
Schlegel
,
A. A.
,
Rudelson
,
J. J.
, &
Tse
,
P. U.
(
2012
).
White matter structure changes as adults learn a second language
.
Journal of Cognitive Neuroscience
,
24
,
1664
1670
.
Scholz
,
J.
,
Klein
,
M. C.
,
Behrens
,
T. E.
, &
Johansen-Berg
,
H.
(
2009
).
Training induces changes in white-matter architecture
.
Nature Neuroscience
,
12
,
1370
1371
.
Schulte-Ruther
,
M.
,
Markowitsch
,
H. J.
,
Fink
,
G. R.
, &
Piefke
,
M.
(
2007
).
Mirror neuron and theory of mind mechanisms involved in face-to-face interactions: A functional magnetic resonance imaging approach to empathy
.
Journal of Cognitive Neuroscience
,
19
,
1354
1372
.
Sherwood
,
C. C.
,
Broadfield
,
D. C.
,
Holloway
,
R. L.
,
Gannon
,
P. J.
, &
Hof
,
P. R.
(
2003
).
Variability of Broca's area homologue in African great apes: Implications for language evolution
.
Anatomical Record
,
271A
,
276
285
.
Subiaul
,
F.
,
Cantlon
,
J. F.
,
Holloway
,
R. L.
, &
Terrace
,
H. S.
(
2004
).
Cognitive imitation in rhesus macaques
.
Science
,
305
,
407
410
.
Taglialatela
,
J. P.
,
Russell
,
J. L.
,
Schaeffer
,
J. A.
, &
Hopkins
,
W. D.
(
2008
).
Communicative signaling activates ‘Broca's’ homolog in chimpanzees
.
Current Biology
,
18
,
343
348
.
Tennie
,
C.
,
Call
,
J.
, &
Tomasello
,
M.
(
2006
).
Push or pull: Imitation vs. emulation in great apes and human children
.
Ethology
,
112
,
1159
1169
.
Tennie
,
C.
,
Call
,
J.
, &
Tomasello
,
M.
(
2009
).
Ratcheting up the ratchet: On the evolution of cumulative culture
.
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
,
364
,
2405
2415
.
Tennie
,
C.
,
Call
,
J.
, &
Tomasello
,
M.
(
2012
).
Untrained chimpanzees (Pan troglodytes schweinfurthii) fail to imitate novel actions
.
PLoS One
,
7
,
e41548
.
Thorndike
,
E. L.
(
1898
).
Animal intelligence: An experimental study of the associative processes in animals
.
Psychological Review: Monograph Supplements
,
2
,
i
109
.
Tomasello
,
M.
(
1996
).
Do apes ape?
In
C. M.
Heyes
&
B. G.
Galef
(Eds.),
Social learning in animals: The roots of culture
(pp.
319
346
).
London
:
Academic Press
.
Tomasello
,
M.
,
Kruger
,
A. C.
, &
Ratner
,
H. H.
(
1993
).
Cultural learning
.
Behavioral and Brain Sciences
,
16
,
495
552
.
Visalberghi
,
E.
, &
Fragaszy
,
D.
(
2002
).
“Do monkeys ape?”—Ten years after
. In
K.
Daughternhahn
&
C. L.
Nehavniv
(Eds.),
Imitation in animals and artifacts
(pp.
471
499
).
Cambridge, MA
:
MIT Press
.
Whiten
,
A.
(
2017
).
Social learning and culture in child and chimpanzee
.
Annual Review of Psychology
,
68
,
129
154
.
Whiten
,
A.
,
McGuigan
,
N.
,
Marshall-Pescini
,
S.
, &
Hopper
,
L. M.
(
2009
).
Emulation, imitation, over-imitation and the scope of culture for child and chimpanzee
.
Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences
,
364
,
2417
2428
.
Williams
,
J. H.
,
Nicolson
,
A. T.
,
Clephan
,
K. J.
,
de Grauw
,
H.
, &
Perrett
,
D. I.
(
2013
).
A novel method testing the ability to imitate composite emotional expressions reveals an association with empathy
.
PLoS One
,
8
,
e61941
.
Zatorre
,
R. J.
,
Fields
,
R. D.
, &
Johansen-Berg
,
H.
(
2012
).
Plasticity in gray and white: Neuroimaging changes in brain structure during learning
.
Nature Neuroscience
,
15
,
528
536
.