Complex Multiplexing of Reward-Cue- and Licking-Movement-Related Activity in Single Midline Thalamus Neurons.

Midline thalamus is implicated in linking visceral and exteroceptive sensory information with behavior. However, whether neuronal activity is modulated with temporal precision by cues and actions in real time is unknown. Using single-neuron recording and a Pavlovian visual-cue/liquid-reward association task in rats, we discovered phasic responses to sensory cues, appropriately timed to modify information processing in output targets, as well as tonic modulations within and between trials that were differentially reward modulated, which may have distinct arousal functions. Many of the cue-responsive neurons also responded to repetitive licks, consistent with sensorimotor integration. Further, some lick-related neurons were activated only by the first rewarded lick and only if that lick were also part of a conditioned response sequence initiated earlier, consistent with binding action decisions to their ensuing outcome. This rich repertoire of responses provides electrophysiological evidence for midline thalamus as a site of complex information integration for reward-mediated behavior. SIGNIFICANCE STATEMENT: Disparate brain circuits are involved in sensation, movement, and reward information. These must interact in order for the relationships between cues, actions, and outcomes to be learned. We found that responses of single neurons in midline thalamus to sensory cues are increased when associated with reward. This output may amplify similar signals generated in parallel by the dopamine system. In addition, some neurons coded a three-factor decision in which the neuron fired only if there was a movement, if it was the first one after the reward becoming available, and if it was part of a sequence triggered in response to a preceding cue. These data highlight midline thalamus as an important node integrating multiple types of information for linking sensation, actions, and rewards.

Intersegmental Interactions Give Rise to a Global Network.

Animal motor behaviors require the coordination of different body segments. Thus the activity of the networks that control each segment, which are distributed along the nerve cord, should be adequately matched in time. This temporal organization may depend on signals originated in the brain, the periphery or other segments. Here we evaluate the role of intersegmental interactions. Because of the relatively regular anatomy of leeches, the study of intersegmental coordination in these animals restricts the analysis to interactions among iterated units. We focused on crawling, a rhythmic locomotive behavior through which leeches move on solid ground. The motor pattern was studied ex vivo, in isolated ganglia and chains of three ganglia, and in vivo. Fictive crawling ex vivo (crawling) displayed rhythmic characteristics similar to those observed in vivo. Within the three-ganglion chains the motor output presented an anterior-posterior order, revealing the existence of a coordination mechanism that occurred in the absence of brain or peripheral signals. An experimental perturbation that reversibly abolished the motor pattern in isolated ganglia produced only a marginal effect on the motor activity recorded in three-ganglion chains. Therefore, the segmental central pattern generators present in each ganglion of the chain lost the autonomy observed in isolated ganglia, and constituted a global network that reduced the degrees of freedom of the system. However, the intersegmental phase lag in the three-ganglion chains was markedly longer than in vivo. This work suggests that intersegmental interactions operate as a backbone of correlated motor activity, but additional signals are required to enhance and speed coordination in the animal.

Output variability across animals and levels in a motor system.

Rhythmic behaviors vary across individuals. We investigated the sources of this output variability across a motor system, from the central pattern generator (CPG) to the motor plant. In the bilaterally symmetric leech heartbeat system, the CPG orchestrates two coordinations in the bilateral hearts with different intersegmental phase relations (Δϕ) and periodic side-to-side switches. Population variability is large. We show that the system is precise within a coordination, that differences in repetitions of a coordination contribute little to population output variability, but that differences between bilaterally homologous cells may contribute to some of this variability. Nevertheless, much output variability is likely associated with genetic and life history differences among individuals. Variability of Δϕ were coordination-specific: similar at all levels in one, but significantly lower for the motor pattern than the CPG pattern in the other. Mechanisms that transform CPG output to motor neurons may limit output variability in the motor pattern.