Dopamine neurons of the monkey midbrain: contingencies of responses to active touch during self-initiated arm movements

“This would dramatically accelerate the (Romo and Schultz 1990).”

“These data might ward-predicting stimuli (which are tested in separate trials) (Romo and Schultz, 1990; Mirenowicz and Schultz,sugggest that phasic dopamine activations reflect attention-inducing properties of stimuli, including rewards, 1994).”

“, 1992) and the triggered task above (Romo and Schultz, 1990; Schultz and Romo, 1990), dopamine neuron responses transferred from reward delivery to sensory cues that predicted reward.”

“(a) Activity of nigral-VTA complex neurons (from Romo & Schultz 1990).”

“Data summarized from Sawaguchi et al. (1986, 1988, 1990a, 1990b), Sawaguchi (2001), Pirot et al.”

“Reward-related stimuli, such as primary liquid and food rewards, and visual and auditory stimuli predicting such rewards elicit pure activations (Romo & Schultz 1990, Schultz & Romo 1990, Ljungberg et al 1992).”

“Some of the behavior-related changes measured by dopamine voltammetry are rarely seen with dopamine impulse activity, in particular the increases following aversive events and during movements in earlier voltammetry studies (Romo & Schultz 1990).”

“…early in the acquisition lated with this motion, the absence of brain regions of lever pressing behavior (Schultz, 1986; Nishino et al., with time course changes specific for cocaine-induced 1987; Romo and Schultz, 1990; Schultz and Romo, 1990; craving is a matter to be interpreted with caution.”

““Unconditioned” liquid or food rewards elicit explicit reward signals in all main components of the brain’s reward system (see FIGURES 7; 8, A–C; 13B; AND 27A) (16, 18, 42, 60, 205, 215, 322, 383, 387, 405, 422, 451, 492, 541, 592).”

“The same neuron responds to the trigger stimulus during the performance of externally triggered movements, and the response to touch of food is no longer present (Romo and Schultz 1990).”

“Hollerman and Schultz, 1998) and when touching food during self-initiated movements (Romo and Schultz, 1990).”

“Dopamine neurons of both areas respond to primary reward during learning or in the absence of predictive stimuli, and to conditioned stimuli predicting reward in an established behavioral sequence (Romo and Schultz, 1990; Schultz and Romo, 1990; Ljungberg et al., 1992).”

“…previous neuroscience studies have focused on the learning aspect of reward anticipation (Hollerman and Schultz, 1998; Mirenowicz and Schultz, 1994; Romo and Schultz, 1990), leaving it unclear whether activation related to reward expectation and risk in subcortical structures requires learning and…”

“Dopamine neurons show activations ('excitations') following reward predicting visual, auditory and somatosensory stimuli (Figure 1B) [31-33].”

“In a seminal series of studies, Schultz and colleagues showed that the firing pattern of phasic dopamine neurons in the macaque ventral tegmental area (VTA) reflects exactly such reward PEs (Romo and Schultz, 1990; Mirenowicz and Schultz, 1994, 1996; Schultz, 1998).”

“DA’s basic roles in approach-related behavior, including effort expenditure (Correa et al, 2002), reinforcement learning (Schultz, 2015), and motor control (Bernheimer et al, 1973; Romo and Schultz, 1990), have been thoroughly covered in the literature and will only be briefly reviewed here.”

“…midbrain DA neurons increased their activity specifically to the unexpected presentation of rewards or conditioned stimuli, whereas such responses were not evident for expected positively reinforcing stimuli, whether conditioned or not (Romo and Schultz, 1990; Schultz et al., 1994; Schultz, 1998).”

“…cues, or both, predicted reward with 100% certainty, the responses of dopamine neurons shifted from the reward itself (as defined above) to the reward-predictive environmental stimuli (Schultz 1986; Romo & Schultz 1990; Ljungberg et al. 1991, 1992; Schultz et al. 1993; Fiorillo et al. 2003).”

“…action potential Ͻ1 ms in duration, which represents the minimum cutoff between DA and slow-firing non-DA cells in recordings with the filter settings commonly used in recordings from conscious rats and monkeys (Schultz, 1986; Romo and Schultz, 1990; Ljungberg et al., 1992; Hyland et al., 2002).”

“However, when learning is complete, if there is no environmental change, neurons become activated only by reward-predicting stimuli and no more by rewards (Romo and Schultz, 1990; Mirenowicz and Schultz, 1994).”

“1989) and dopamine impulse activity (Romo and Schultz 1990).”

“Data are from Romo and Schultz (1990). relative to their prediction, rather than signaling rewards unconditionally.”

“1983; Tremblay and Schultz 1999, 2000a,b), the midbrain dopamine nuclei (Ljungberg et al. 1991, 1992; Mirenowicz and Schultz 1994; Romo and Schultz 1990; Schultz et al. 1993a), the lateral hypothalamus (Burton et al.”

“75 The short-latency response of dopamine neurons to primary rewards and conditioned, reward-predicting stimuli 42,46,60,62,66 might constitute a biological implementation of a TD reinforcement signal.”

“Dopaminergic neurons in the mesencephalon can be activated both by primary food and fluid rewards and by conditioned incentive stimuli predicting reward (Schultz, 1986; Romo and Schultz, 1990; Ljungberg et al., 1992).”

“Instead, midbrain DA neurons are activated specifically in situations with a reward value, whether elicited by conditioned or unconditioned stimuli (Schultz, 1986; Nishino et al., 1987; Romo and Schultz, 1990; Ljungberg etal., 1991).”

“These include the unexpected presentation of rewards (Romo and Schultz, 1990; Mirenowicz and Schultz, 1996), conditioned stimuli (Mirenowicz and Schultz, 1994), discriminative stimuli (Miller et al., 1981), and novelty (Steinfels et al., 1983; Freeman and Bunney , 1987; Ljungberg et al., 1992).”

“They show phasic, but not sustained, activations after unpredicted rewards and conditioned, reward-predicting stimuli, and they are depressed when a predicted reward is omitted (Ljungberg et al. 1992; Mirenowicz and Schultz 1994; Romo and Schultz 1990; Schultz et al. 1993).”

“However, it is consistent with the paucity of movement-related activity in dopamine cells in monkeys [15–19], rats [20 ,21,22], or cats [23], and imaging studies in humans that indicate responses to reward in the striatum [24–26].”

“Interestingly, these neurons are capable of distinguishing between reward and nonreward objects (Romo and Schultz, 1990) and to respond to aversive stimuli with a decreased spontaneous activity (Schultz et al.”

“They do not show comparable premovement activity (Romo and Schultz 1990) and thus do not actively participate in the development of preparatory activity in loops.”

“Slower electrophysiological dopamine changes occur with movements (Schultz et al. 1983; Schultz 1986; Romo and Schultz 1990), but are sluggish and inconsistent and often fail to occur in better controlled behavioral tasks (DeLong et al. 1983; Schultz and Romo 1990; Ljungberg et al. 1992; Waelti et…”

“These cellular phenotypes recapitulate the classic concept that, in mammals, single spikes firing in DA neurons are thought to play a permissive role in initiating movements (Romo and Schultz, 1990), while burst firing is correlated with arousal states and motivation.”

“This pacemaking activity is believed to be important in maintaining ambient DA levels in regions that are innervated by these neurons, particularly the striatum (Romo and Schultz, 1990).”

“Extracellular recordings from midbrain dopamine neurons reveal initial phasic activity in response to unpredicted reward delivery (Hollerman and Schultz, 1998; Ljungberg et al., 1992; Romo and Schultz, 1990; Schultz, 1998a, b; Schultz et al., 1997).”

“Dopaminergic neurons projecting to the caudate-putamen show a high incidence of reward-related activity associated with the expectation and receipt of reward (Ljungberg et al., 1992; Romo and Schultz, 1990; Schultz and Romo, 1990).”

“This pacemaking activity is believed to be important in maintaining ambient DA levels in regions that are innervated by these neurons, particularly the striatum [38].”

“…neurons also regulate midbrain DA neurons, an operation that is consistent with behavioral state control, given that midbrain DA neuronal activity has been associated with behavioral activation and response to novel stimuli (Romo and Schultz, 1990; Schultz and Romo, 1990; Ljungberg et al., 1992).”

“Durations of 1 ms represent the typical cutoff between DA and slow-firing non-DA cells under these recording conditions in both rats and monkeys (Schultz, 1986; Romo and Schultz, 1990; Ljungberg et al., 1992; Hyland et al., 2002).”

“SNpc neurons are able to generate action potentials in the absence of synaptic input (Romo and Schultz, 1990).”

“Dopaminergic neurons increase in firing rate when an animal touches food [78;79] and when liquid reward is administered to the animal outside of a behavioral context [77].”

“Conversely, the relative stability of dorsolateral striatal DA release in response to changes in firing rate is consistent with the hypothesis that DA release in the dorsal striatum enables the initiation of cognitive and motor responses but does not necessarily correlate with the induction of movement (Romo and Schul…”

“…error signal used in animal learning (Schultz et al., 1997; Schultz, 1996; Schultz et al., 1993; Mirenowicz & Schultz, 1994; Ljungberg et al., 1992; Romo & Schultz, 1990; Schultz, 1986), (2) the evidence linking dopamine to learning (Rammsayer, 1999; Kumari et al., 1997; Dobkin & Hanlon, 1993;…”

“[106] Romo R, Schultz W.”

“Similar activations occur when these movements occur spontaneously (12%) in a design that addressed the most impaired movement type in Parkinsonism [52].”

“In primates, presentation of different foods and sweet solutions, or visual and auditory stimuli paired previously with reward results in brief, phasic firing of DA neurons in the VTA (Romo & Schultz, 1990; Schultz & Romo, 1990; Ljungberget al., 1992).”

“…although unexpected, are nonetheless congruent with electrophysiological evidence that similar changes in VTA DA cell activity are associated with food reinforcement (Schultz, 1986; Nishino et al., 1987; Romo and Schultz, 1990; Schultz and Romo, 1990; Ljungberg et al., 1992; Schultz et al., 1993).”

“…striatum (VS), and NAcc neurons of moderately trained monkeys were activated during prereward incentive-related events (Nishino et al., 1987; Romo and Schultz, 1990; Apicella et al., 1992; Ljungberg et al., 1992; Schultz et al., 1992) (for related findings in rats, see Carelli and…”

“Early reports suggested that some dopamine neurons have small changes in tonic activity in anticipation of arm movements to obtain food rewards (Romo and Schultz, 1990) or delivery of probabilistic rewards (Fiorillo et al., 2003), but these changes have not always been reported in later studies…”

“…Durham, NC 27708, USA hy43@duke.edu Received: 12 April 2015 Accepted: 06 May 2015 Published: 27 May 2015 Citation: Barter JW, Li S, Lu D, Bartholomew RA, Rossi MA, Shoemaker CT, Salas-Meza D, Gaidis E and Yin HH (2015) Beyond reward prediction errors: the role of dopamine in movement kinematics.”

“This pacemaking activity is believed to be important to maintaining ambient DA levels in regions that are innervated by these neurons, particularly the striatum (102).”