Biology subjects

Gothard, K. M.

Publications and source records attributed to Gothard, K. M..

8 recordsLinked to original sources

bioRxiv2025

Uncertainty Shapes Neural Dynamics in Motor Cortex During Reaching

Voluntary reaching movements are often made with incomplete information about the movement goal, which may require the brain to flexibly adjust motor plans and ongoing movements. To examine how uncertainty about a reach target influences neural preparation and execution, we recorded activity from dorsal premotor (PMd) and primary motor (M1) cortices of a rhesus macaque trained to reach to one of two potential targets. In the task, a timing cue flashed three times in succession. Potential targets were displayed at the time of the first flash and the monkey needed to initiate the movement almost simultaneously with the third flash. Colorings of potential targets indicated the probability that the target would be at one location or the other, thereby inducing varying levels of uncertainty about the final target location. On half the trials, the final target was displayed so late that the monkey had to guess the target location, based on cues provided by the potential targets. While the monkey performed this task, we recorded 165 neurons from PMd and 37 from M1. Population neural trajectories in the preparatory subspace of PMd (but not M1) were progressively less expansive with higher levels of uncertainty. Despite differences in preparatory states associated with uncertainty, the movements produced were the same. The narrower separation between states suggested a neural-based explanation for more rapid movement re-preparation with higher uncertainty. Furthermore, we found a dimension in neural state-space representing the level of uncertainty during movement preparation and execution. SIGNIFICANCE STATEMENTThe dorsal premotor cortex (PMd) in primates plays a critical role in organizing preparatory states needed for the execution of target-directed movements mediated downstream by the primary motor cortex (M1). But what if the location of the target is uncertain - as often occurs in our daily lives, such as reaching for a pair of glasses in the dark that have fallen to the floor. We found that different levels of uncertainty are clearly represented in population neural activity during preparation for movement in monkey PMd but not M1. Furthermore, these different neural states related to uncertainty were not associated with changes in the movements produced. These findings provide further insight (and questions) about the operations of the motor cortex.

neuroscience↗

bioRxiv2024

Social Status as a Latent Variable in the Amygdala of Observers of Social Interactions

Successful integration into a hierarchical social group requires knowledge of the status of each individual and of the rules that govern social interactions within the group. In species that lack morphological indicators of status, social status can be inferred by observing the signals exchanged between individuals. We simulated social interactions between macaques by juxtaposing videos of aggressive and appeasing displays where two individuals appeared in each others line of sight and their displays were timed to suggest the reciprocation of dominant and subordinate signals. Viewers of these videos successfully inferred the social status of the interacting characters. Dominant individuals attracted more social attention from viewers even when they were not engaged in social displays. Neurons in the viewers amygdala signaled the status of both the attended (fixated) and the unattended individuals suggesting that in third party observers of social interactions, the amygdala signals jointly the status of interacting parties. HighlightsO_LIMonkeys infer the social status of conspecifics from videos of simulated dyadic interactions C_LIO_LIDuring fixations neural populations signal the social status of the attended individuals C_LIO_LINeurons in the amygdala jointly encode the status of interacting individuals C_LI In briefThird party-viewers of pairwise dominant-subordinate interactions infer social status from the observed behaviors. Neurons in the amygdala are tuned to the inferred dominant/subordinate status of both individuals.

animal behavior and cognition↗

bioRxiv2024

Interoceptive Signals Bias Decision Making in Rhesus Macaques

Several influential theories have proposed that interoceptive signals, sent from the body to the brain, contribute to neural processes that coordinate complex behaviors. We altered the physiological state of the body using compounds that have minimal effect on the brain and evaluated their effect on decision-making in rhesus monkeys. We used glycopyrrolate, a non-specific muscarinic (parasympathetic) antagonist, and isoproterenol, a beta-1/2 (sympathetic) agonist, to create a sympathetic-dominated state in the periphery, that was indexed by increased heart rate. Rhesus monkeys were trained on two variants of an approach-avoidance conflict task. The tasks offered a choice between enduring mildly aversive stimuli in exchange for a steady flow of rewards, or cancelling the aversive stimuli, forgoing the rewards. The delay to interrupt the aversive stimuli was used as a measure of monkeys tolerance for contact with a hot but not painful stimulus or airflow directed at their muzzle. Both drugs reduced tolerance for the aversive stimuli. To determine whether the drug-induced autonomic state reduced the subjective value of the reward, we tested the effects of glycopyrrolate on a food preference task. Food preference was unaltered, suggesting that the sympathetic dominated state in the periphery selectively reduces tolerance for aversive stimuli without altering reward-seeking behaviors. As the drugs used are expected to have little or no direct effect on the brain, the observed biases in decision making are likely induced by interoceptive afferents that signal to the brain the physiological state of the body. Significance statementThe brain adjusts body physiology to the behavioral agenda of the organism through autonomic efferents; concomitantly interoceptive afferents carry signals that inform the brain about the physiological state of the body, closing a homeostatic regulatory loop. Persuasive theories proposed that interoceptive afferents contribute to higher cognitive functions, including emotion. Empirical evidence that these signals are sufficient to bias complex behavior has been limited by the difficulty of isolating interoceptive afferents from the rest of the homeostatic loop. Here we selectively manipulated the autonomic state of the body using drugs with limited penetrance of the brain in macaques performing decision-making tasks. Sympathetic-dominated peripheral states significantly altered decision making, suggesting that changes in interoceptive afferent signals are sufficient to bias behavior.

neuroscience↗

bioRxiv2024

Detection of latent brain states from baseline neural activity in the amygdala

The amygdala responds to a large variety of socially and emotionally salient environmental and interoceptive stimuli. The context in which these stimuli occur determines their social and emotional significance. In canonical neurophysiological studies, the fast-paced succession of stimuli and events induce phasic changes in neural activity. During inter-trial intervals neural activity is expected to return to a stable and relatively featureless baseline. Context, such as the presence of a social partner, or the similarity of trials in a blocked design, induces brain states that can transcend the fast-paced succession of stimuli and can be recovered from the baseline firing rate of neurons. Indeed, the baseline firing rates of neurons in the amygdala change between blocks of trials of gentle grooming touch, delivered by a trusted social partner, and non-social airflow stimuli, delivered by a computer-controlled air valve. In this experimental paradigm, the presence of the groomer alone was sufficient to induce small but significant changes in baseline firing rates. Here, we examine local field potentials (LFP) recorded during these baseline periods to determine whether context was encoded by network dynamics that emerge in the local field potentials from the activity of large ensembles of neurons. We found that machine learning techniques can reliably decode social vs. non-social context from spectrograms of baseline local field potentials. Notably, decoding accuracy improved significantly with access to broad-band information. No significant differences were detected between the nuclei of the amygdala that receive direct or indirect inputs from areas of the prefrontal cortex known to coordinate flexible, context-dependent behaviors. The lack of nuclear specificity suggests that context-related synaptic inputs arise from a shared source, possibly interoceptive inputs that signal the sympathetic- vs. parasympathetic-dominated states characterizing non-social and social blocks, respectively.

neuroscience↗

bioRxiv2024

Brainwide mesoscale functional networks revealed by focal infrared neural stimulation of the amygdala

The primate amygdala serves to evaluate emotional content of sensory inputs and modulate emotional and social behaviors; it modulates cognitive, multisensory and autonomic circuits predominantly via the basal (BA), lateral (LA), and central (CeA) nuclei, respectively. Based on recent electrophysiological evidence suggesting mesoscale (millimeters-scale) nature of intra-amygdala functional organization, we have investigated the connectivity of these nuclei using Infrared Neural Stimulation of single mesoscale sites coupled with mapping in ultrahigh field 7T functional Magnetic Resonance Imaging (INS-fMRI). Stimulation of multiple sites within amygdala of single individuals evoked mesoscale functional connectivity maps, allowing comparison of BA, LA and CeA connected brainwide networks. This revealed a mesoscale nature of connected sites, complementary spatial patterns of functional connectivity, and topographic relationships of nucleus-specific connections. Our data reveal a functional architecture of systematically organized brainwide networks mediating sensory, cognitive, and autonomic influences from the amygdala.

neuroscience↗

bioRxiv2022

A context-dependent switch from sensing to feeling in the primate amygdala

The skin transmits affective signals that integrate into our social vocabulary. As the socio-affective aspects of touch are likely processed in the amygdala, we compared neural responses to social grooming and gentle airflow recorded from the amygdala and the primary somatosensory cortex of non-human primates. Neurons in the somatosensory cortex responded to both types of tactile stimuli. In the amygdala, however, neurons did not respond to individual grooming sweeps even though grooming elicited autonomic states indicative of positive affect. Instead, many showed changes in baseline firing rates that persisted throughout the grooming bout. Such baseline fluctuations were attributed to social context because the presence of the groomer alone could account for the observed changes in baseline activity. It appears, therefore, that during grooming, the amygdala stops responding to external inputs on a short time scale but remains responsive to social context (or the associated affective states) on longer time scales.

neuroscience↗

bioRxiv2021

Automatic recognition of macaque facial expressions for detection of affective states

Internal 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 Facial Action Coding System (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 recognition of six dominant AUs, generalizing between conspecific individuals (Macaca mulatta) and even between species (Macaca fascicularis). 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.

neuroscience↗

bioRxiv2020

Mesoscopic-scale functional networks in the primate amygdala

The primate amygdala performs multiple functions that may be related to the anatomical heterogeneity of its nuclei. At the level of single neurons, each function is reflected in stimulus- and task-specific responses. Given that neurons with a particular response profile are not clustered in any of the nuclei, 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 (Macaca mulatta) 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.

neuroscience↗