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.
Highlights
Active neurons (TANs) constitute a group of neurons in the striatum that are readily identified by their spiking characteristics in electrophysiological studies performed in behaving animals (Apicella, 2002)
We found that the Tonically active neurons (TANs) sampled all displayed, on average, stronger responses to rewarding events in ventral than dorsal striatum, with specific response features occurring in the ventral striatum
We classified recorded striatal neurons into TANs on the basis of well-established electrophysiological characteristics, including tonic irregular spontaneous firing rates, long-duration spike waveforms, and changes in activity during task performance expressed as brief decreases in firing in response to rewarding events (Kimura et al, 1984; Aosaki et al, 1994; Apicella et al, 1997)
Summary
Active neurons (TANs) constitute a group of neurons in the striatum that are readily identified by their spiking characteristics in electrophysiological studies performed in behaving animals (Apicella, 2002). Behaving monkey experiments have led to the prevailing view that TANs carry signals that are important for implementing reward-guided learning (Aosaki et al, 1994; Apicella et al, 1997; Ravel et al, 2003; Morris et al, 2004; Adler et al, 2013) In this regard, responses of TANs and midbrain DA neurons to motivationally salient events are quite similar (Apicella, 2007), notwithstanding differences in the polarity of their modulation. Some TANs display a decrease in activity after reward delivery and an increase in activity when reward is omitted, possibly reflecting differential coding of the presence and absence of upcoming reward (Apicella et al, 2009) These TAN modulations have been evidenced in dorsal regions of the monkey striatum. It cannot be excluded that the group identified as TANs in the rodent striatum may contain some non-cholinergic neurons (Beatty et al, 2012) exhibiting distinct response profiles during task performance
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