We have recorded neural activity from the amygdala and somatosensory cortex in response to alternating blocks of non-social and social tactile stimuli. The social stimuli consisted of grooming-like finger sweeps delivered by a trusted human to the monkey's face. For non-social stimuli, we used gentle airpuffs delivered to multiple regions of the face, avoiding the eyes, nostrils, and ears.
When groomed by a conspecific, monkeys close their eyes and often fall asleep, relinquishing attention and vigilance to the groomer. Our subjects demonstrated a similar response. Their state of relaxation and low vigilance was indicated by low-frequency and high amplitude activity in the cortical local field potentials. These cortical states directly correlated with decreases in heart rate and increases in heart rate variability. When the monkeys had sufficient experience with alternating blocks of grooming and air puffs, their heart rate changed in anticipation of the upcoming blocks.
As expected, neurons in the somatosensory cortex responded to both non-social and social stimuli, differentiating between locations and contact pressures. Consistent with our previous studies (Mosher et al., 2016, Morrow et al., 2019), approximately 30% of neurons in the amygdala responded to non-social tactile stimuli. Contrary to our expectations, however, < 10% of the same neurons responded to social touch, even when the social touch was delivered with comparable pressure and to the same areas of the skin. The failure of neurons to respond to social touch suggests a 'gating' mechanism, possibly explained by one or more of the following:
- Neurons in the amygdala respond weakly to external stimuli during states of low vigilance. High vigilance is characterized by high gamma oscillations in the amygdala that entrain and increase the spiking activity of the resident neurons (Amir et al., 2018). During low-vigilance states elicited by grooming, the amygdala may switch from monitoring the external environment to monitoring an internal state. Decoupling the amygdala from external stimuli results in gating phasic responses to tactile stimuli. Because typical neural recordings require animals to remain vigilant and engage with external stimuli, such gating in the amygdala has not been previously reported. It is well known that the amygdala plays a pivotal role in vigilance and attention (Davis and Whalen 2001), showing enhanced and almost automatic facilitation of attention for threat-related stimuli (Le Doux, 2007, Vuilleumier, 2005).
- It is also possible that during vagal tone (an autonomic state dominated by parasympathetic activity), neurotransmitters and neuromodulators released in the amygdala lower the excitability and/or responsivity of neurons to external stimuli. Indeed, the small fraction of neurons that responded to both social and non-social touch were active when the heart rate remained high across the blocks.
- Context neurons may inhibit touch-responsive neurons. During grooming blocks, a subset of neurons in the amygdala showed tonic changes in firing rate persisting for the entire duration of the block. These neurons increased their activity at the time of switching from the non-social to the social touch, anticipating the period of grooming. We have no evidence that these context neurons have an inhibitory effect on touch-responsive neurons, but when these neurons are not simultaneously active.
- Unpredictable stimuli are more likely to elicit responses than predictable stimuli. During these predictable periods of grooming, neurons in the amygdala did not respond to grooming sweeps. However, when these sweeps were unexpected, neurons that failed to respond during the touch blocks showed a detectable response.