Dynamics and potential significance of spontaneous activity in the habenula

Abstract

The habenula is an evolutionarily conserved structure of the vertebrate brain that is essential for behavioural flexibility and mood control. It is spontaneously active and is able to access diverse states when the animal is exposed to sensory stimuli. Here we investigate the dynamics of habenula spontaneous activity, to gain insight into how sensitivity is optimized. Two-photon calcium imaging was performed in resting zebrafish larvae at single cell resolution. An analysis of avalanches of inferred spikes suggests that the habenula is subcritical. Activity had low covariance and a small mean, arguing against dynamic criticality. A multiple regression estimator of autocorrelation time suggests that the habenula is neither fully asynchronous nor perfectly critical, but is reverberating. This pattern of dynamics may enable integration of information and high flexibility in the tuning of network properties, thus providing a potential mechanism for the optimal responses to a changing environment. Significance Statement: Spontaneous activity in neurons shapes the response to stimuli. One structure with a high level of spontaneous neuronal activity is the habenula, a regulator of broadly acting neuromodulators involved in mood and learning. How does this activity influence habenula function? We show here that the habenula of a resting animal is near criticality, in a state termed reverberation. This pattern of dynamics is consistent with high sensitivity and flexibility, and may enable the habenula to respond optimally to a wide range of stimuli.