Differences between Dorsal and Ventral Striatum in the Sensitivity of Tonically Active Neurons to Rewarding Events

Abstract

Within the striatum, cholinergic interneurons, electrophysiologically identified as tonically active neurons (TANs), represent a relatively homogeneous group in terms of their functional properties. They display typical pause in tonic firing in response to rewarding events which are of crucial importance for reinforcement learning. These responses are uniformly distributed throughout the dorsal striatum (i.e., motor and associative striatum), but it is unknown, at least in monkeys, whether differences in the modulation of TAN activity exist in the ventral striatum (i.e., limbic striatum), a region specialized for processing of motivational information. To address this issue, we examined the activity of dorsal and ventral TANs in two monkeys trained on a Pavlovian conditioning task in which a visual stimulus preceded the delivery of liquid reward by a fixed time interval. We found that the proportion of TANs responding to the stimulus predictive of reward did not vary significantly across regions (58%–80%), whereas the fraction of TANs responding to reward was higher in the limbic striatum (100%) compared to the motor (65%) and associative striatum (52%). By examining TAN modulation at the level of both the population and the individual neurons, we showed that the duration of pause responses to the stimulus and reward was longer in the ventral than in the dorsal striatal regions. Also, the magnitude of the pause was greater in ventral than dorsal striatum for the stimulus predictive of reward but not for the reward itself. We found similar region-specific differences in pause response duration to the stimulus when the timing of reward was less predictable (fixed replaced by variable time interval). Regional variations in the duration and magnitude of the pause response were transferred from the stimulus to reward when reward was delivered in the absence of any predictive stimulus. It therefore appears that ventral TANs exhibit stronger responses to rewarding stimuli, compared to dorsal TANs. The high proportion of responsive neurons, combined with particular response features, support the notion that the ventral TAN system can be driven by specific synaptic inputs arising from afferent sources distinct from those targeting the dorsal TAN system.

Temporal Coding of Reward Value in Monkey Ventral Striatal Tonically Active Neurons

“…). The pause-pulse nature of TANs responses has become almost diagnostic for their identification (Marche et al, 2017) and is frequently used as one of the criteria to identify TANs. For at least some of the reward offerings each of our TANs showed the pause followed by an excitatory rebound response that has been taken as characteristic of TANs (Kimura et al, 1984(Kimura et al, , 1990Apicella, 2002Apicella, , 2017.…”

“…At this point it is not clear whether the phase reversing responses we have seen are characteristic of TANs throughout the striatum, and they can only be seen when there is a wide range of values to encode, or whether they are found only in this limbic striatum. In monkeys the one study that compares TANs in the dorsal, intermediate, and ventral striatum shows that the dorsal and ventral TANs have differences in response latency and pause width in response to rewarding events (Marche et al, 2017), so it is at least plausible to think this could be a characteristic found only in limbic striatum, but it is possible that the reversing modulation we have seen in ventral TANs is also a feature of dorsal TANs response, if they were to be recorded under the same experimental circumstances.…”

“…Most of what we know about the activity of TANs in monkeys comes from studies of the dorsal part of the striatum Apicella et al, 1997Apicella et al, , 2011Ravel et al, 2006;Nougaret and Ravel, 2015). To date there seems to have been only one recording study of TANs in monkeys that specifically included ventral striatum (Marche et al, 2017). We determined how the discounted value of rewards is coded by TANs in the rostromedioventral striatum, using a visually-cued multi-drop/multidelay reward task.…”

Subthalamic nucleus and globus pallidus interna influence firing of tonically active neurons in the primate striatum through different mechanisms

“…. The responsive TANs were mainly located in the dorsolateral region of the putamen and in the region that is posterior to the anterior commissure; these areas correspond to known sensorimotor areas of the putamen (Parent & Hazrati, ; Haber, ; Marche et al ., ).…”

Shared striatal activity in decisions to satisfy curiosity and hunger at the risk of electric shocks

“…These findings dovetail with the notion that the ventral striatum computes the value of the stimulus ('critic') while the dorsal striatum plays a role in selecting an action/response ('actor') 50 . Several empirical studies provided supportive evidence for the idea but were all limited to extrinsic incentives 51,52,65 . Our findings suggest that 21 the neural computation of curiosity-based decision-making can possibly be understood within the actor-critic model of reinforcement learning.…”