Katalin M Gothard
- Professor, Physiology
- Assistant Professor, Neurobiology
- Assistant Professor, Evelyn F Mcknight Brain Institute
- Assistant Professor, BIO5 Institute
- Associate Professor, Neurology
- Associate Professor, Physiological Sciences - GIDP
- Member of the Graduate Faculty
- Ph.D. Neuroscience
- the Universiry of Arizona, Tucson, Arizona, USA
- Multiple Maps and Multiple Spatial Reference Frames in the Rat Hippocampus
- Timisoara Medical School, Timisoara, Romania
- U of A College of Medicine (2015 - Ongoing)
- U of A College of Medicine (2009 - 2015)
- Universiry of Arizona (2009 - 2015)
- U of A Collge and Medicine (2002 - 2009)
- College of Medicine (2002 - 2009)
- UC Davis (2000 - 2002)
- Center for Neuroscience, CNPRC (1998 - 2000)
- ARL-NSMA The Universiry of Arizona (1996 - 1998)
- University of Arizona, Graduate Interdisciplinary Program (1990 - 1996)
- University Hospital (1988 - 1990)
- Executive Committee of Simian Collective
- Fall 2022
- Elected member - Dana Alliance or Brain Initiative
- Dana Foundation, Fall 2019
- Exellence in teaching in year 1 COM
- College of Medicine, Spring 2018
- Kavli Fellow
- National Academy of Science, Fall 2014
Licensure & Certification
- MD, Timisoara Medical School (1988)
Systems Neurophysiology;Human Neuroanatomy and Neurophysiology;Autonomic neurophysiology;Social and emotional behavior in mammals;
The neural basis of emotion and social behavior in primates
Directed ResearchNSCS 492 (Spring 2023)
DissertationNRSC 920 (Spring 2023)
Honors Independent StudyACBS 399H (Spring 2023)
Honors Independent StudyACBS 499H (Spring 2023)
Honors ThesisNSCS 498H (Spring 2023)
ResearchNRSC 900 (Spring 2023)
ResearchPS 900 (Spring 2023)
Systems NeuroscienceNRSC 560 (Spring 2023)
Directed ResearchNROS 492 (Fall 2022)
Directed ResearchPSIO 492 (Fall 2022)
DissertationNRSC 920 (Fall 2022)
Honors Directed ResearchNROS 392H (Fall 2022)
Honors Directed ResearchNROS 492H (Fall 2022)
Honors Independent StudyACBS 399H (Fall 2022)
Honors Independent StudyACBS 499H (Fall 2022)
Honors Independent StudyPSIO 399H (Fall 2022)
Honors ThesisNSCS 498H (Fall 2022)
ResearchNRSC 900 (Fall 2022)
ResearchPS 900 (Fall 2022)
Honors Directed ResearchNSCS 392H (Summer I 2022)
Honors Independent StudyACBS 399H (Summer I 2022)
Honors Directed ResearchNSCS 392H (Spring 2022)
Honors Directed ResearchNSCS 492H (Spring 2022)
Honors Independent StudyACBS 399H (Spring 2022)
ResearchNRSC 900 (Spring 2022)
ResearchPS 900 (Spring 2022)
Systems NeuroscienceNRSC 560 (Spring 2022)
Honors Directed ResearchNSCS 492H (Fall 2021)
ResearchNRSC 900 (Fall 2021)
Rsrch Meth Psio SciPS 700 (Fall 2021)
Honors Directed ResearchNSCS 492H (Summer I 2021)
Methods In NeuroscienceNRSC 700 (Spring 2021)
Systems NeuroscienceNRSC 560 (Spring 2021)
Directed ResearchNSCS 492 (Fall 2020)
Directed ResearchPSIO 492 (Fall 2020)
ResearchNRSC 900 (Fall 2020)
Directed ResearchPSIO 492 (Spring 2020)
Methods In NeuroscienceNRSC 700 (Spring 2020)
Systems NeuroscienceNRSC 560 (Spring 2020)
Methods In NeuroscienceNRSC 700 (Fall 2019)
Directed RsrchMCB 392 (Spring 2019)
DissertationNRSC 920 (Spring 2019)
Honors Directed ResearchNSCS 492H (Spring 2019)
Senior CapstoneNSCS 498 (Spring 2019)
Systems NeuroscienceNRSC 560 (Spring 2019)
Directed ResearchNSCS 392 (Fall 2018)
DissertationNRSC 920 (Fall 2018)
Honors Directed ResearchNSCS 392H (Fall 2018)
Senior CapstoneNSCS 498 (Fall 2018)
DissertationNRSC 920 (Spring 2018)
Systems NeuroscienceNRSC 560 (Spring 2018)
Directed ResearchNSCS 492 (Fall 2017)
DissertationNRSC 920 (Fall 2017)
Methods In NeuroscienceNRSC 700 (Fall 2017)
Directed ResearchNSCS 492 (Spring 2017)
DissertationNRSC 920 (Spring 2017)
Honors ThesisNSCS 498H (Spring 2017)
Independent StudyPSIO 399 (Spring 2017)
ResearchNRSC 900 (Spring 2017)
Systems NeuroscienceNRSC 560 (Spring 2017)
DissertationNRSC 920 (Fall 2016)
Honors ThesisNSCS 498H (Fall 2016)
ResearchNRSC 900 (Fall 2016)
Directed ResearchNSCS 492 (Spring 2016)
Honors Independent StudyNSCS 499H (Spring 2016)
ResearchNRSC 900 (Spring 2016)
Systems NeuroscienceNRSC 560 (Spring 2016)
- Champ, T. M., Lee, S., Martin, A. B., Bolles, C. M., Kim, S. W., & Gothard, K. M. (2022). Social engagement revealed by gaze following in third-party observers of simulated social conflict. Frontiers in psychology, 13, 952390.More infoHumans and non-human primates can allocate visual attention to areas of high interest in their visual field based on the behaviors of their social partners. Allocation of attention is particularly important for third-party observers of social interactions. By following the gaze of interacting individuals, the observer can obtain information about the mental states, emotions, and intentions of others. We presented three adult monkeys () with videos of simulated social interactions and quantified their eye movements to determine which observed behaviors were most conducive to gaze following. Social interactions were simulated by juxtaposing two videos depicting a threatening and an appeasing individual facing each other, with the timing of the facial and bodily displays adjusted to mimic an exchange of social signals. Socially meaningful facial displays combined with full body movements significantly enhanced the probability of gaze following and joint attention. Despite the synthetic nature of these interactions, the facial and bodily displays of the submissive individual elicited significantly more joint-attention than gaze-following saccades, suggesting a preferential allocation of attention to the recipients of threatening displays. Temporal alignment of gaze following and joint attention to the frames of each video showed numerous clusters of significant increases in the frequency of these saccades. These clusters suggest that some videos contained signals that can induce a quasi-automatic redirection of the observer's attention. However, these saccades occurred only on a fraction of the viewings, and we have documented large inter-individual variations. All viewers produced sequences of joint attention saccades (check-backs) shifting their attention between the two monkeys as though monitoring the simulated emitting-receiving cycle of social signals. These sequences reflect the viewer's interest in monitoring the ongoing exchange of agonistic and affiliative displays. It appears that in macaque monkeys, the scanpaths of third-party observers of simulated social interactions are informed by social-cognitive processes suggestive of mentalizing.
- Gothard, K. M. (2022). Marmosets confirm that context is king. Neuron, 110(8), 1273-1274.More infoNeural responses to vocalizations are expected to depend on the sensory features of the stimulus. In this issue of Neuron, Jovanovic and colleagues show that call-responsive neurons in the prefrontal cortex of marmosets signal not only the auditory stimulus but also the social-behavioral context.
- Gothard, K. M., & Fuglevand, A. J. (2022). The role of the amygdala in processing social and affective touch. Current opinion in behavioral sciences, 43, 46-53.More infoThe amygdala plays a central role in emotion and social behavior, yet its role in processing social and affective touch is not well established. Longitudinal studies reveal that touch-deprived infants show later in life exaggerated emotional reactivity related to structural and functional changes in the amygdala and other brain structures. The internal organization and connectivity of the amygdala is well-suited to process the sensory features of tactile stimuli and also the socio-cognitive dimensions of the received touch. The convergent processing of bottom-up and top-down pathways that carry information about touch results in the elaboration of context appropriate autonomic responses. Indeed, the positive value of affective touch in humans and social grooming in non-human primates is correlated with vagal tone and the release of oxytocin and endogenous opioids. Grooming, the non-human primate equivalent of affective touch in humans, reduces vigilance, that depends on the amygdala. During touch-induced vagal tone and low vigilance, neural activity in the amygdala is substantially different from activity corresponding to the attentive processing of tactile stimuli. Under these circumstances neurons no longer respond phasically to each touch stimulus, rather they signal a sustained functional state in which the amygdala appears decoupled from monitoring the external environment.
- Hasse, B. A., Sheets, D. E., Holly, N. L., Gothard, K. M., & Fuglevand, A. J. (2022). Restoration of complex movement in the paralyzed upper limb. Journal of neural engineering, 19(4).More infoFunctional electrical stimulation (FES) involves artificial activation of skeletal muscles to reinstate motor function in paralyzed individuals. While FES applied to the upper limb has improved the ability of tetraplegics to perform activities of daily living, there are key shortcomings impeding its widespread use. One major limitation is that the range of motor behaviors that can be generated is restricted to a small set of simple, preprogrammed movements. This limitation stems from the substantial difficulty in determining the patterns of stimulation across many muscles required to produce more complex movements. Therefore, the objective of this study was to use machine learning to flexibly identify patterns of muscle stimulation needed to evoke a wide array of multi-joint arm movements.. Arm kinematics and electromyographic (EMG) activity from 29 muscles were recorded while a 'trainer' monkey made an extensive range of arm movements. Those data were used to train an artificial neural network that predicted patterns of muscle activity associated with a new set of movements. Those patterns were converted into trains of stimulus pulses that were delivered to upper limb muscles in two other temporarily paralyzed monkeys.. Machine-learning based prediction of EMG was good for within-subject predictions but appreciably poorer for across-subject predictions. Evoked responses matched the desired movements with good fidelity only in some cases. Means to mitigate errors associated with FES-evoked movements are discussed.. Because the range of movements that can be produced with our approach is virtually unlimited, this system could greatly expand the repertoire of movements available to individuals with high level paralysis.
- Holly, N. L., Hasse, B. A., Gothard, K. M., & Fuglevand, A. J. (2022). Large-scale intramuscular electrode system for chronic electromyography and functional electrical stimulation. Journal of neurophysiology, 128(4), 1011-1024.More infoTo understand how the central nervous system (CNS) enacts movements, it seems important to monitor the activities of the many muscles involved. Likewise, to restore complex movements to paralyzed limbs with electrical stimulation requires access to most limb muscles. Intramuscular electrodes are needed to obtain isolated recordings or stimulation of individual muscles. As such, we developed and tested the stability of large arrays of implanted intramuscular electrodes. We implanted 58 electrodes in 29 upper limb muscles in each of three macaques. Electrode connectors were protected within a skull-mounted chamber. During surgery, wires were tunneled subcutaneously to target muscles, where gold anchors were crimped onto the leads. The anchors were then deployed with an insertion device. In two monkeys, the chamber was fixed to the skull with a titanium baseplate rather than acrylic cement. In multiple sessions up to 15 wk after surgery, electromyographic (EMG) signals were recorded while monkeys made the same reaching movement. EMG signals were stable, with an average (SD) coefficient of variation across sessions of 0.24 ± 0.15. In addition, at 4, 8, and 16 wk after surgery, forces to incrementing stimulus pulses were measured for each electrode. The threshold current needed to evoke a response at 16 wk was not different from that at 4 wk. Likewise, peak force evoked by 16 mA of current at 16 wk was not different from 4 wk. The stability of this system implies it could be effectively used to monitor and stimulate large numbers of muscles needed to understand the control of natural and evoked movements. A new method was developed to enable long-lasting recording and stimulation of large numbers of muscles with intramuscular electrodes. Electromyographic signals and evoked force responses in 29 upper limb muscles remained stable over several months when tested in nonhuman primates. This system could be used effectively to monitor and stimulate numerous muscles needed to more fully understand the control of natural and evoked movements.
- Morozov, A., Parr, L. A., Gothard, K., Paz, R., & Pryluk, R. (2022). Automatic Recognition of Macaque Facial Expressions for Detection of Affective States. eNeuro, 8(6).More infoInternal affective states produce external manifestations such as facial expressions. In humans, the Facial Action Coding System (FACS) is widely used to objectively quantify the elemental facial action units (AUs) that build complex facial expressions. A similar system has been developed for macaque monkeys-the Macaque FACS (MaqFACS); yet, unlike the human counterpart, which is already partially replaced by automatic algorithms, this system still requires labor-intensive coding. Here, we developed and implemented the first prototype for automatic MaqFACS coding. We applied the approach to the analysis of behavioral and neural data recorded from freely interacting macaque monkeys. The method achieved high performance in the recognition of six dominant AUs, generalizing between conspecific individuals () and even between species (). The study lays the foundation for fully automated detection of facial expressions in animals, which is crucial for investigating the neural substrates of social and affective states.
- Gothard, K. M. (2017). Bridging the gap between rodents and humans: The role of non-human primates in oxytocin research. American Journal of Primatology.
- Shi, S., Xu, A. G., Rui, Y. Y., Zhang, X., Romanski, L. M., Gothard, K. M., & Roe, A. W. (2021). Infrared neural stimulation with 7T fMRI: A rapid in vivo method for mapping cortical connections of primate amygdala. NeuroImage, 231, 117818.More infoWe have previously shown that INS-fMRI is a rapid method for mapping mesoscale brain networks in the macaque monkey brain. Focal stimulation of single cortical sites led to the activation of connected cortical locations, resulting in a global connectivity map. Here, we have extended this method for mapping brainwide networks following stimulation of single subcortical sites. As a testbed, we focused on the basal nucleus of the amygdala in the macaque monkey. We describe methods to target basal nucleus locations with submillimeter precision, pulse train stimulation methods, and statistical tests for assessing non-random nature of activations. Using these methods, we report that stimulation of precisely targeted loci in the basal nucleus produced sparse and specific activations in the brain. Activations were observed in the insular and sensory association cortices as well as activations in the cingulate cortex, consistent with known anatomical connections. What is new here is that the activations were focal and, in some cases, exhibited shifting topography with millimeter shifts in stimulation site. The precision of the method enables networks mapped from different nearby sites in the basal nucleus to be distinguished. While further investigation is needed to improve the sensitivity of this method, our analyses do support the reproducibility and non-random nature of some of the activations. We suggest that INS-fMRI is a promising method for mapping large-scale cortical and subcortical networks at high spatial resolution.
- Gothard, K. M. (2020). Multidimensional processing in the amygdala. Nature reviews. Neuroscience, 21(10), 565-575.More infoBrain-wide circuits that coordinate affective and social behaviours intersect in the amygdala. Consequently, amygdala lesions cause a heterogeneous array of social and non-social deficits. Social behaviours are not localized to subdivisions of the amygdala even though the inputs and outputs that carry social signals are anatomically restricted to distinct subnuclear regions. This observation may be explained by the multidimensional response properties of the component neurons. Indeed, the multitudes of circuits that converge in the amygdala enlist the same subset of neurons into different ensembles that combine social and non-social elements into high-dimensional representations. These representations may enable flexible, context-dependent social decisions. As such, multidimensional processing may operate in parallel with subcircuits of genetically identical neurons that serve specialized and functionally dissociable functions. When combined, the activity of specialized circuits may grant specificity to social behaviours, whereas multidimensional processing facilitates the flexibility and nuance needed for complex social behaviour.
- Morrow, J. K., Cohen, M. X., & Gothard, K. M. (2020). Mesoscopic-scale functional networks in the primate amygdala. eLife, 9.More infoThe primate amygdala performs multiple functions that may be related to the anatomical heterogeneity of its nuclei. Individual neurons with stimulus- and task-specific responses are not clustered in any of the nuclei, suggesting that single-units may be too-fine grained to shed light on the mesoscale organization of the amygdala. We have extracted from local field potentials recorded simultaneously from multiple locations within the primate () amygdala spatially defined and statistically separable responses to visual, tactile, and auditory stimuli. A generalized eigendecomposition-based method of source separation isolated coactivity patterns, or components, that in neurophysiological terms correspond to putative subnetworks. Some component spatial patterns mapped onto the anatomical organization of the amygdala, while other components reflected integration across nuclei. These components differentiated between visual, tactile, and auditory stimuli suggesting the presence of functionally distinct parallel subnetworks.
- Putnam, P. T., & Gothard, K. M. (2020). Multidimensional Neural Selectivity in the Primate Amygdala. eNeuro, 6(5).More infoThe amygdala contributes to multiple functions including attention allocation, sensory processing, decision-making, and the elaboration of emotional behaviors. The diversity of functions attributed to the amygdala is reflected in the response selectivity of its component neurons. Previous work claimed that subsets of neurons differentiate between broad categories of stimuli (e.g., objects vs faces, rewards vs punishment), while other subsets are narrowly specialized to respond to individual faces or facial features (e.g., eyes). Here we explored the extent to which the same neurons contribute to more than one neural subpopulation in a task that activated multiple functions of the amygdala. The subjects () watched videos depicting conspecifics or inanimate objects, and learned by trial and error to choose the individuals or objects associated with the highest rewards. We found that the same neurons responded selectively to two or more of the following task events or stimulus features: (1) alerting, task-related stimuli (fixation icon, video start, and video end); (2) reward magnitude; (3) stimulus categories (social vs nonsocial); and (4) stimulus-unique features (faces, eyes). A disproportionate number of neurons showed selectivity for all of the examined stimulus features and task events. These results suggest that neurons that appear specialized and uniquely tuned to specific stimuli (e.g., face cells, eye cells) are likely to respond to multiple other types of stimuli or behavioral events, if/when these become behaviorally relevant in the context of a complex task. This multidimensional selectivity supports a flexible, context-dependent evaluation of inputs and subsequent decision making based on the activity of the same neural ensemble.
- Burgos-Robles, A., Gothard, K. M., Monfils, M. H., Morozov, A., & Vicentic, A. (2019). Conserved features of anterior cingulate networks support observational learning across species. Neuroscience and biobehavioral reviews, 107, 215-228.More infoThe ability to observe, interpret, and learn behaviors and emotions from conspecifics is crucial for survival, as it bypasses direct experience to avoid potential dangers and maximize rewards and benefits. The anterior cingulate cortex (ACC) and its extended neural connections are emerging as important networks for the detection, encoding, and interpretation of social signals during observational learning. Evidence from rodents and primates (including humans) suggests that the social interactions that occur while individuals are exposed to important information in their environment lead to transfer of information across individuals that promotes adaptive behaviors in the form of either social affiliation, alertness, or avoidance. In this review, we first showcase anatomical and functional connections of the ACC in primates and rodents that contribute to the perception of social signals. We then discuss species-specific cognitive and social functions of the ACC and differentiate between neural activity related to 'self' and 'other', extending into the difference between social signals received and processed by the self, versus observing social interactions among others. We next describe behavioral and neural events that contribute to social learning via observation. Finally, we discuss some of the neural mechanisms underlying observational learning within the ACC and its extended network.
- Morrow, J., Mosher, C., & Gothard, K. (2019). Multisensory Neurons in the Primate Amygdala. The Journal of neuroscience : the official journal of the Society for Neuroscience, 39(19), 3663-3675.More infoAnimals identify, interpret, and respond to complex, natural signals that are often multisensory. The ability to integrate signals across sensory modalities depends on the convergence of sensory inputs at the level of single neurons. Neurons in the amygdala are expected to be multisensory because they respond to complex, natural stimuli, and the amygdala receives inputs from multiple sensory areas. We recorded activity from the amygdala of 2 male monkeys () in response to visual, tactile, and auditory stimuli. Although the stimuli were devoid of inherent emotional or social significance and were not paired with rewards or punishments, the majority of neurons that responded to these stimuli were multisensory. Selectivity for sensory modality was stronger and emerged earlier than selectivity for individual items within a sensory modality. Modality and item selectivity were expressed via three main spike-train metrics: (1) response magnitude, (2) response polarity, and (3) response duration. None of these metrics were unique to a particular sensory modality; rather, each neuron responded with distinct combinations of spike-train metrics to discriminate sensory modalities and items within a modality. The relative proportion of multisensory neurons was similar across the nuclei of the amygdala. The convergence of inputs of multiple sensory modalities at the level of single neurons in the amygdala rests at the foundation for multisensory integration. The integration of visual, auditory, and tactile inputs in the amygdala may serve social communication by binding together social signals carried by facial expressions, vocalizations, and social grooming. Our brain continuously decodes information detected by multiple sensory systems. The emotional and social significance of the incoming signals is likely extracted by the amygdala, which receives input from all sensory domains. Here we show that a large portion of neurons in the amygdala respond to stimuli from two or more sensory modalities. The convergence of visual, tactile, and auditory signals at the level of individual neurons in the amygdala establishes a foundation for multisensory integration within this structure. The ability to integrate signals across sensory modalities is critical for social communication and other high-level cognitive functions.
- Doane, C. J., Zimmerman, P. E., Putnam, P. T., Gothard, K. M., & Besselsen, D. G. (2018). Silicon foreign body in the cerebrum of a rhesus macaque (Macaca mulatta). Comparative Medicine, 68(2), 1-5.
- Gothard, K. M., Mosher, C. P., Zimmerman, P. E., Putnam, P. T., Morrow, J. K., & Fuglevand, A. J. (2018). New perspectives on the neurophysiology of primate amygdala emerging from the study of naturalistic social behaviors. Wiley interdisciplinary reviews. Cognitive science, 9(1).More infoA major challenge of primate neurophysiology, particularly in the domain of social neuroscience, is to adopt more natural behaviors without compromising the ability to relate patterns of neural activity to specific actions or sensory inputs. Traditional approaches have identified neural activity patterns in the amygdala in response to simplified versions of social stimuli such as static images of faces. As a departure from this reduced approach, single images of faces were replaced with arrays of images or videos of conspecifics. These stimuli elicited more natural behaviors and new types of neural responses: (1) attention-gated responses to faces, (2) selective responses to eye contact, and (3) selective responses to touch and somatosensory feedback during the production of facial expressions. An additional advance toward more natural social behaviors in the laboratory was the implementation of dyadic social interactions. Under these conditions, neurons encoded similarly rewards that monkeys delivered to self and to their social partner. These findings reinforce the value of bringing natural, ethologically valid, behavioral tasks under neurophysiological scrutiny. WIREs Cogn Sci 2018, 9:e1449. doi: 10.1002/wcs.1449 This article is categorized under: Psychology > Emotion and Motivation Neuroscience > Cognition Neuroscience > Physiology.
- Putnam, P. T., Young, L. J., & Gothard, K. M. (2018). Bridging the gap between rodents and humans: The role of non-human primates in oxytocin research. American journal of primatology, 80(10), e22756.More infoOxytocin (OT), a neuropeptide that acts in the brain as a neuromodulator, has been long known to shape maternal physiology and behavior in mammals, however its role in regulating social cognition and behavior in primates has come to the forefront only in the recent decade. Many of the current perspectives on the role of OT in modulating social behavior emerged first from studies in rodents, where invasive techniques with a high degree of precision have permitted the mechanistic dissection of OT-related behaviors, as well as their underlying neural circuits in exquisite detail. In parallel, behavioral and imaging studies in humans have suggested that brain OT may similarly influence human social behavior and neural activity. These studies in rodents and humans have spurred interest in the therapeutic potential of targeting the OT system to remedy deficits in social cognition and behavior that are present across numerous psychiatric disorders. Yet there remains a tremendous gap in our mechanistic understanding of the influence of brain OT on social neural circuitry between rodents and man. In fact, very little is known regarding the neural mechanisms by which exogenous or endogenous OT influences human social cognition, limiting its therapeutic potential. Here we discuss how non-human primates (NHPs) are uniquely positioned to now bridge the gaps in knowledge provided by the precise circuit-level approaches widely used in rodent models and the behavioral, imaging, and clinical studies in humans. This review provides a perspective on what has been achieved, and what can be expected from exploring the role of OT in shaping social behaviors in NHPs in the coming years.
- Gothard, K. M. (2017). New perspectives on the neurophysiology of primate amygdala emerging from the study of naturalistic social behaviors. Wiley Interdisciplinary Review in Cognitive Sciene, 9(1). doi:10.1002/wcs
- Minxha, J., Mosher, C., Morrow, J. K., Mamelak, A. N., Adolphs, R., Gothard, K. M., & Rutishauser, U. (2017). Fixations Gate Species-Specific Responses to Free Viewing of Faces in the Human and Macaque Amygdala. Cell reports, 18(4), 878-891.More infoNeurons in the primate amygdala respond prominently to faces. This implicates the amygdala in the processing of socially significant stimuli, yet its contribution to social perception remains poorly understood. We evaluated the representation of faces in the primate amygdala during naturalistic conditions by recording from both human and macaque amygdala neurons during free viewing of identical arrays of images with concurrent eye tracking. Neurons responded to faces only when they were fixated, suggesting that neuronal activity was gated by visual attention. Further experiments in humans utilizing covert attention confirmed this hypothesis. In both species, the majority of face-selective neurons preferred faces of conspecifics, a bias also seen behaviorally in first fixation preferences. Response latencies, relative to fixation onset, were shortest for conspecific-selective neurons and were ∼100 ms shorter in monkeys compared to humans. This argues that attention to faces gates amygdala responses, which in turn prioritize species-typical information for further processing.
- Ballesta, S., Mosher, C. P., Szep, J., Fischl, K. D., & Gothard, K. M. (2016). Social determinants of eyeblinks in adult male macaques. Scientific reports, 6, 38686.More infoVideos with rich social and emotional content elicit natural social behaviors in primates. Indeed, while watching videos of conspecifics, monkeys engage in eye contact, gaze follow, and reciprocate facial expressions. We hypothesized that the frequency and timing of eyeblinks also depends on the social signals contained in videos. We monitored the eyeblinks of four male adult macaques while they watched videos of conspecifics displaying facial expressions with direct or averted gaze. The instantaneous blink rate of all four animals decreased during videos. The temporal synchrony of blinking, however, increased in response to segments depicting appeasing or aggressive facial expressions directed at the viewer. Two of the four monkeys, who systematically reciprocated the direct gaze of the stimulus monkeys, also showed eyeblink entrainment, a temporal coordination of blinking between social partners engaged in dyadic interactions. Together, our results suggest that in macaques, as in humans, blinking depends not only on the physiological imperative to protect the eyes and spread a film of tears over the cornea, but also on several socio-emotional factors.
- Mosher, C. P., Zimmerman, P. E., Fuglevand, A. J., & Gothard, K. M. (2016). Tactile Stimulation of the Face and the Production of Facial Expressions Activate Neurons in the Primate Amygdala. eNeuro, 3(5).More infoThe majority of neurophysiological studies that have explored the role of the primate amygdala in the evaluation of social signals have relied on visual stimuli such as images of facial expressions. Vision, however, is not the only sensory modality that carries social signals. Both humans and nonhuman primates exchange emotionally meaningful social signals through touch. Indeed, social grooming in nonhuman primates and caressing touch in humans is critical for building lasting and reassuring social bonds. To determine the role of the amygdala in processing touch, we recorded the responses of single neurons in the macaque amygdala while we applied tactile stimuli to the face. We found that one-third of the recorded neurons responded to tactile stimulation. Although we recorded exclusively from the right amygdala, the receptive fields of 98% of the neurons were bilateral. A fraction of these tactile neurons were monitored during the production of facial expressions and during facial movements elicited occasionally by touch stimuli. Firing rates arising during the production of facial expressions were similar to those elicited by tactile stimulation. In a subset of cells, combining tactile stimulation with facial movement further augmented the firing rates. This suggests that tactile neurons in the amygdala receive input from skin mechanoceptors that are activated by touch and by compressions and stretches of the facial skin during the contraction of the underlying muscles. Tactile neurons in the amygdala may play a role in extracting the valence of touch stimuli and/or monitoring the facial expressions of self during social interactions.
- Putnam, P. T., Roman, J. M., Zimmerman, P. E., & Gothard, K. M. (2016). Oxytocin enhances gaze-following responses to videos of natural social behavior in adult male rhesus monkeys. Psychoneuroendocrinology, 72, 47-53.More infoGaze following is a basic building block of social behavior that has been observed in multiple species, including primates. The absence of gaze following is associated with abnormal development of social cognition, such as in autism spectrum disorders (ASD). Some social deficits in ASD, including the failure to look at eyes and the inability to recognize facial expressions, are ameliorated by intranasal administration of oxytocin (IN-OT). Here we tested the hypothesis that IN-OT might enhance social processes that require active engagement with a social partner, such as gaze following. Alternatively, IN-OT may only enhance the perceptual salience of the eyes, and may not modify behavioral responses to social signals. To test this hypothesis, we presented four monkeys with videos of conspecifics displaying natural behaviors. Each video was viewed multiple times before and after the monkeys received intranasally either 50 IU of OT or saline. We found that despite a gradual decrease in attention to the repeated viewing of the same videos (habituation), IN-OT consistently increased the frequency of gaze following saccades. Further analysis confirmed that these behaviors did not occur randomly, but rather predictably in response to the same segments of the videos. These findings suggest that in response to more naturalistic social stimuli IN-OT enhances the propensity to interact with a social partner rather than merely elevating the perceptual salience of the eyes. In light of these findings, gaze following may serve as a metric for pro-social effects of oxytocin that target social action more than social perception.
- Burke, S. N., Thome, A., Plange, K., Engle, J. R., Trouard, T. P., Gothard, K. M., & Barnes, C. A. (2014). Orbitofrontal cortex volume in area 11/13 predicts reward devaluation, but not reversal learning performance, in young and aged monkeys. The Journal of Neuroscience, 34(30), 9905-16.More infoThe orbitofrontal cortex (OFC) and amygdala are both necessary for decisions based on expected outcomes. Although behavioral and imaging data suggest that these brain regions are affected by advanced age, the extent to which aging alters appetitive processes coordinated by the OFC and the amygdala is unknown. In the current experiment, young and aged bonnet macaques were trained on OFC- and amygdala-dependent tasks that test the degree to which response selection is guided by reward value and can be adapted when expected outcomes change. To assess whether the structural integrity of these regions varies with levels of performance on reward devaluation and object reversal tasks, volumes of areas 11/13 and 14 of the OFC, central/medial (CM), and basolateral (BL) nuclei of the amygdala were determined from high-resolution anatomical MRIs. With age, there were significant reductions in OFC, but not CM and BL, volume. Moreover, the aged monkeys showed impairments in the ability to associate an object with a higher value reward, and to reverse a previously learned association. Interestingly, greater OFC volume of area 11/13, but not 14, was significantly correlated with an animal's ability to anticipate the reward outcome associated with an object, and smaller BL volume was predictive of an animal's tendency to choose a higher value reward, but volume of neither region correlated with reversal learning. Together, these data indicate that OFC volume has an impact on monkeys' ability to guide choice behavior based on reward value but does not impact ability to reverse a previously learned association.
- Gothard, K. M. (2014). The amygdalo-motor pathways and the control of facial expressions. Frontiers in neuroscience, 8, 43.More infoFacial expressions reflect decisions about the perceived meaning of social stimuli and the expected socio-emotional outcome of responding (or not) with a reciprocating expression. The decision to produce a facial expression emerges from the joint activity of a network of structures that include the amygdala and multiple, interconnected cortical and subcortical motor areas. Reciprocal transformations between these sensory and motor signals give rise to distinct brain states that promote, or impede the production of facial expressions. The muscles of the upper and lower face are controlled by anatomically distinct motor areas. Facial expressions engage to a different extent the lower and upper face and thus require distinct patterns of neural activity distributed across multiple facial motor areas in ventrolateral frontal cortex, the supplementary motor area, and two areas in the midcingulate cortex. The distributed nature of the decision manifests in the joint activation of multiple motor areas that initiate the production of facial expression. Concomitantly multiple areas, including the amygdala, monitor ongoing overt behaviors (the expression itself) and the covert, autonomic responses that accompany emotional expressions. As the production of facial expressions is brought into the framework of formal decision making, an important challenge will be to incorporate autonomic and visceral states into decisions that govern the receiving-emitting cycle of social signals.
- Mosher, C. P., Zimmerman, P. E., & Gothard, K. M. (2014). Neurons in the monkey amygdala detect eye contact during naturalistic social interactions. Current Biology, 24(20), 2459-64.More infoPrimates explore the visual world through eye-movement sequences. Saccades bring details of interest into the fovea, while fixations stabilize the image. During natural vision, social primates direct their gaze at the eyes of others to communicate their own emotions and intentions and to gather information about the mental states of others. Direct gaze is an integral part of facial expressions that signals cooperation or conflict over resources and social status. Despite the great importance of making and breaking eye contact in the behavioral repertoire of primates, little is known about the neural substrates that support these behaviors. Here we show that the monkey amygdala contains neurons that respond selectively to fixations on the eyes of others and to eye contact. These "eye cells" share several features with the canonical, visually responsive neurons in the monkey amygdala; however, they respond to the eyes only when they fall within the fovea of the viewer, either as a result of a deliberate saccade or as eyes move into the fovea of the viewer during a fixation intended to explore a different feature. The presence of eyes in peripheral vision fails to activate the eye cells. These findings link the primate amygdala to eye movements involved in the exploration and selection of details in visual scenes that contain socially and emotionally salient features.
- Gothard, K. M. (2021, August). From sensing to feeling; Is the swich in the amygdala?. The Zanvyl Krieger Mind/Brain Institute Johns Hopkins University THE DAVID BODIAN VIRTUAL SEMINAR. Johns Hopkins UNiversity: The Zanvyl Krieger Mind/Brain Institute Johns Hopkins University.
- Gothard, K. M. (2021, August). Multidimensional Processing in the Primate Amygdala. Cedars Sinai Neuroscience lectures. Cedar Sinai Hospital Los Angeles: Cedars Sinai Hospital.
- Gothard, K. M. (2021, Jan). Where and how is social status represented in the brain. Neuoscience GIDP. Tucson: GIDp Neuroscience.
- Gothard, K. M. (2021, October). From sensing to feeling; Is the swich in the amygdala?. Center for Cognitive Neuroscience Colloquium series. Duke University.
- Gothard, K. M. (2021, October). The role of the amygdala in processing social and affective touch.. Invited lecture. New York Univesity, Ichan School of Medicine: Ichan School of Medicine.
- Gothard, K. M. (2021, September). From sensing to feeling; Is teh swich in the amygdala. Cognitive Neuroscience Lecture Series. Psychology Department University of Arizona: Cognitive Neuroscience.
- Gothard, K. M. (2020, August). From Discriminative to Affective Touch. UC Irvine lecture series.
- Gothard, K. M. (2020, Janaury). A new view of the amygdala; insights from multidimentional processing. Neurology Grant Rounds.
- Gothard, K. M. (2020, July). From Discriminative to Affective Touch: COrtico-amygdala Processing loops. Federation of European Neuroscience Societies, Glasgow, 2020.
- Gothard, K. M. (2020, June). FRom DIscriminative to Affective Touch. Rodboud University, The Netherlands.
- Gothard, K. M. (2019, April). Multidimensinal neural selectivity in the monkey amygdala. Psychology seminar series. Emory University: Dept of Psychology, Emory University.
- Gothard, K. M. (2019, August). A role of the primate amygdala in social and afective touch. Gordn research Conference. Stonehill College MA: Gordon Research Conferences.
- Gothard, K. M. (2019, February). The Mind-Body Dialoge. U of A Science Lecture Series. U of A campus: Centennial Hall: Collge of Science.
- Gothard, K. M. (2019, March). Multidimensional responses in the monkey amgdala; what is hiding in the hidden layer?. Emerging neurotechnologies in non-human primats, Shenzhen, China. Shenzhen, China: MIT.More infoThis was an invited lecture in a forum of neurotechnolgies for non-human primates
- Gothard, K. M. (2019, October). Neural Correlates of social Engagement elicited in Rhesus monkeys by videos with social content. Annual Meeting of the Society for Neuroscience. Chicago, IL: Society for Neuroscience.
- Gothard, K. M. (2019, September). An amygdala-centered neuroethological approach to social behavior. International School of Brain Evolution, Erice, Italy. Erice, Italy: International School of Brain Evolution.
- Gothard, K. M. (2019, September). From sensing to feeling in the primate amygdala. International Association for the Study of Affective Touch. Linkoping Sweden: Linkoping University.
- Gothard, K. M. (2019, September). From sensing to feeling; a somatosensory pathway to the amygdala. European Brain and Behavior Society. Prague, the Czech Republic: European Brain and Behavior Society.
- Gothard, K. M. (2016, Fall). The Magic of Emotional Touch. Distinctive Voices. UC Irvine: National Academy of Sciences.
- Gothard, K. M. (2016, Spring semester). Science Cafe public lecture in Tucson. Science Cafe. Tucson: University of Arizona.More infoDowntown Science Cafe @ Magpie's Gourmet Pizza
- Gothard, K. M. (2016, Summer). Lecture for Tucson Harvard CLub. Tucson Harvard Club. Tucson: Tucson Harvard Club.
- Gothard, K. M. (2016, Summer). Tactile stimulation of the face and the production of facial expressions activate neurons in the primate amygdala. Gordon Research Conference, The Neurobiology of Cognition,. Sunday River, ME: Gordon research Conferences.
- Gothard, K. M. (2016, summer). Attentional selection gates responses of face-selective cells in the human and macaque amygdala. 30-th Center for Visual Science Symposium, University of RochesterUniversity of Rochester.
- Gothard, K. M., Mosher, C. P., Zimmerman, P. E., & Fuglevand, A. J. (2016, May). The neural basis of the receiving-emitting cycle of facial expressions in macaques. The Neuroscience of Emotion. Erice Italy: University of Parma.
- Gothard, K. M. (2015, August). The social functions of the primate amygdala. Gordon Research Conference - The Amygdala in Health and Disease. Stonehill College MA: Gordon Research Conferences.More infohttps://www.grc.org/programs.aspx?id=13511
- Gothard, K. M. (2015, July). Close-loop computations in the social circuits of the primate brain. Telluride workshop on Neuromorhic engineering. Telluride CO: National Science Froundation.More infohttp://www.neuromorphs.net/nm/wiki/2015
- Gothard, K. M. (2015, July). Social cognition in rhesus macaQUES. NEUREX meeting on "Cognition in Primates". Strasbourg, France: NEUREX.More infohttp://www.neurex.org/event/meeting-cognition-of-primates/The editors of Brain and Behavioral Sciences invited the speakers at this conference to contribute to a special issues of the journal. I will have to submit an article to this journal in August 2016.
- Gothard, K. M. (2015, June). Neural circuits of emotion and social cognition in hte primate brain. Intenatinal Summer school of Cognitive Neuroscience, Lyonn, France. Lyonn, France: CNRS France (equivalent to NIH, USA).More infoI gave four lectures to faculty and students at this summer school.
- Gothard, K. M. (2015, October). The Neurophysiology of social cognition in rhesus macaQUES. Association of Primate Veterinarians Workshop. Scottsdale AZ: Assoiation of Primate Veterinarians.More infohttps://www.primatevets.org/workshop
- Gothard, K. M. (2014, December). Naturalistic social stimuli elicit eye-selective neural responses in the monkey amygdala. Seminar Series of the Scientific Director of the National Institute of Mental Health. Washington DC: National Institute of Mental Health.
- Gothard, K. M. (2014, October). Oxytocin enhances social behaviors in macaques. Annual Meeting of the Society for Social Neuroscience. Washington DC: Society for Social Neuroscience.
- Gothard, K. M. (2014, Spring semester). The role of the primate amygdala in the receiving-emitting cycle of facial expressions. Research Seminar at the Vision Center University of Rochester. Rochester: University of Rochester.
- Gothard, K. M. (2014, fall). Primate models of emotion and social behavior. Kavli Frontiers of Science. Beijing, CHIna: National Academy of Science.
- Gothard, K. M. (2014, fall). The eyes: a window to the social brain. Johns Hopkins University: Special conference on neural recordings from the human brain.
- Gothard, K. M. (2014, summer). The central role of the amygdala in social behavior. International Workshop of Neuromorphic Engineering. Telluride, Colorado: UC San Diego.
- Gothard, K. M. (2019, October). Amygdalo-cortical networks revealed by high-field fMRI during infrared neural stimulation of amygdalar subnuclei in the macaque monkey. Annuala meeting of the Society for Neuroscience. Chicago, IL: SFN.
- Gothard, K. M. (2019, October). Blinks punctuate the sequence of cognitive states required by a social learning task. Society for Social Neuroscience. Chicago, IL: Society for Social Neuroscience.
- Gothard, K. M. (2019, October). From discriminative to affective touch: a single-unit perspective of the somatosensory pathway to the amygdala. Society for Neuroscience. Chicago, IL: SFN.
- Gothard, K. M. (2019, October). Statistically separable components of the local field potential show sensory-modality specific spike-field coherence in the primate amygdala. Annual Meeting of the Society for Neuroscience. Chicago, IL: SFN.
- Gothard, K. M. (2019, October). The touch-processing pathway from the somatosensory cortex and the amygdala; a mezoscale perspective. SFN. Chicago, IL: SFN.