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

Martin, A.; Cardenas, Michael A; Andersen, Rose K.; Bowman, Archer  I.; Hillier, Elizabeth A.; Bensmaı̈a, Sliman J.; Fuglevand, Andrew J.; Gothard, Katalin M.

doi:10.1016/j.celrep.2023.112056

Cited by 7 publications

(6 citation statements)

References 97 publications

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“…Therefore, another possibility is that the visual stimulation previously paired, during past reallife grooming, with C-afferent stimulation, produced, through a process akin to pattern completion, the same pleasant sensations and bodily states. Such effects could be mediated through multimodal limbic structures such as the insula and amygdala, that are involved in the processing of pleasant touch in humans and monkeys [29][30][31][32][33] .…”

Section: Discussionmentioning

confidence: 99%

Virtual social grooming in macaques and its psychophysiological effects

Disarbois,

Duhamel

2024

Sci Rep

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Allogrooming is a widespread, pervasive activity among non-human primates. Besides its hygienic function, it is thought to be instrumental in maintaining social bonds and establishing hierarchical structures within groups. However, the question arises as to whether the physiological and social benefits derived from social touch stem directly from body stimulation, or whether other mechanisms come into play. We address this question by analyzing an elaborate social behavior that we observed in two adult male macaques. This behavior demonstrates the existence of a persistent motivation to interact through a form of simulated grooming, as the animals were housed in adjacent enclosures separated by a glass panel preventing direct tactile contact. We find that such virtual grooming produces similar physiological sensations and social effects as allogrooming. We suggest that this behavior engages affective and reward brain circuits to the same extent as real social touch, and that this is probably achieved through high level processes similar to those involved in bodily illusions or synaesthetic phenomena previously described in humans. This observation reveals the unsuspected capacity of non-human primates to invent alternative, quasi-symbolic strategies to obtain effects similar to those provided by direct bodily interaction, which are so important for maintaining social bonds.

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Section: Discussionmentioning

confidence: 99%

Virtual social grooming in macaques and its psychophysiological effects

Disarbois,

Duhamel

2024

Sci Rep

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“…For a detailed description of the experiment and data collection, see the Methods section of Martin et. al.…”

Section: Methodsmentioning

confidence: 99%

“…Both CNN and SVM leverage statistical methods to nonlinearly transform baseline spectrograms and "learn" spatiotemporal patterns (features) that separate airflow from touch in this new feature space. Given that context-related modulation was seen in a fraction of the single units (Martin et al, 2023), we hypothesize that baseline LFP, which records from a larger population of neurons at the mesoscale, may provide a more reliable feature space for successfully decoding context than single-units.…”

Section: Machine Learning For Lfp Analysismentioning

confidence: 99%

“…Indeed, affective states, such as anxiety, persist longer than an emotional reaction to the negatively or positively valanced external stimulus. We have recently demonstrated that grooming, the most common form of social and affective touch in macaques, elicits persistent changes in baseline firing rate in 25-45% of neurons in the amygdala (Martin et al, 2023). The observed changes in baseline were correlated with the animal’s physiological state (low sympathetic and high parasympathetic tone) and with the social context.…”

Section: Introductionmentioning

confidence: 99%

“…As the LFP in each nucleus (subjected to common reference averaging to eliminate volume-conducted components), result from the synaptic currents received and summed across thousands of neurons (Buzsáki et al, 2012; Pesaran et al, 2018), the LFP in the basal and accessory basal nuclei may be driven by inputs from the primate-specific areas of the prefrontal cortex that enable context-dependent flexible emotional behaviors (Passingham and Wise, 2012). Alternatively, the context-related activity may arise from interoceptive inputs, signaling to the brain the parasympathetic-dominated physiological state observed during the grooming blocks (Martin et al, 2023). In this case, we expect comparable decoding accuracy from all nuclei of the amygdala.…”

Section: Introductionmentioning

confidence: 99%

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

Aucoin,

Lin,

Gothard

2024

Preprint

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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.

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The big mixup: Neural representation during natural modes of primate visual behavior

Leopold

2024

Current Opinion in Neurobiology

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

Cited by 7 publications

References 97 publications

Virtual social grooming in macaques and its psychophysiological effects

Virtual social grooming in macaques and its psychophysiological effects

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

The big mixup: Neural representation during natural modes of primate visual behavior

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