Responses of tonically active neurons in the monkey striatum discriminate between motivationally opposing stimuli - PubMed (original) (raw)
Responses of tonically active neurons in the monkey striatum discriminate between motivationally opposing stimuli
Sabrina Ravel et al. J Neurosci. 2003.
Abstract
The striatum is involved in the control of appetitively motivated behavior. We found previously that tonically active neurons (TANs) in the monkey striatum show discriminative responses to different stimuli that are appetitive or aversive. However, these differential responses may reflect the sensory qualities of the stimulus rather than its motivational value. In the present study, we sought to define more precisely the relationship between the particular aspect of the response of TANs and the motivational value of stimuli. For this purpose, three monkeys were presented with two types of aversive stimuli (loud sound and air puff) and one appetitive stimulus (fruit juice). In most instances, the TAN responses to the loud sound and the air puff were similar, in terms of response pattern and duration, whereas responses to the liquid reward showed distinct features. Using classical appetitive conditioning, we reversed the motivational value of a stimulus so that a previously aversive stimulus was now associatively paired with a reward and found that this manipulation selectively modifies the expression of TAN responses to the stimulus. These data indicate that the characteristics of neuronal responses undergo modifications when the valence of the stimulus is changed from aversive to appetitive during associative learning, suggesting that TANs may contribute to a form of stimulus encoding that is dependent on motivational attributes. The adaptation of TAN responses such as observed in the present study likewise reflects a neuronal system that adjusts to the motivational information about environmental events.
Figures
Figure 1.
Responses to aversive and appetitive stimuli in three TANs. Each dot represents a neuronal impulse, and each line of dots represents the neuronal activity recorded during a trial. Histograms and dot displays of neuronal activity are aligned on the onset of stimuli. The neurons for which the activity is shown in a and b responded to all three stimuli but displayed a different pattern of responses between aversive (left and middle) and appetitive (right) stimuli. The response to the air puff of the neuron shown in b was larger than to the loud sound. One example of a neuron responding selectively to aversive stimuli is shown in c. Vertical calibration on histograms is in impulses per bin. Bin width for histograms is 10 msec.
Figure 2.
Population response histograms of TANs tested with aversive and appetitive stimuli. N, Number of neurons included for each histogram.
Figure 3.
Lack of relation of TAN responses to behavioral reactions evoked by aversive stimuli. a, Independence of neuronal responses from individual eye movements elicited by the loud sound in one TAN. Same conventions as in Figure 1. Data were collected when the loud sound was repeatedly presented during a block of trials (left) and were separated offline according to presence or absence of eye movements (right). Superimposed traces of horizontal electrooculograms recorded simultaneously in the same trials (middle). b, Percentage of eye movements evoked by two aversive stimuli (left). Separate symbols are used to show block percentage of eye movement reactions recorded for the loud sound and the faint noise associated with air-puff delivery. Total percentage of responding neurons (middle). Population responses of TANs to the two aversive stimuli (right). Number of neurons included for each histogram (middle and right) are as follows: loud sound, 30 neurons; faint noise, 23 neurons.
Figure 4.
Positions of tonically active neurons with different response selectivities in the three monkeys. Recording sites of neurons tested with all three stimuli are plotted on standard coronal sections labeled in rostrocaudal stereotaxic planes. loud sound and airpuff + liquid reward, Responses to all three stimuli; loud sound or airpuff + liquid reward, neurons responding to the delivery of juice and to at least one of the aversive stimuli; loud sound and/or airpuff, selective responses to aversive stimuli; liquid reward, selective responses to the delivery of juice.
Figure 5.
Learning curves for the stimulus–reward association on one monkey. Each point indicates the percentage of licks starting before reward delivery compared with the total number of trials by block (top) and the latency of licks (bottom) for each block.
Figure 6.
Neuronal correlates of learning of associations between aversive stimuli and reward. a, Changes of representative responses to the auditory stimulus and reward of three TANs recorded during successive training periods. Conventions are similar to those in Figure 1. Superimposed traces of licking movement records aligned on the onset of the auditory stimulus are shown at the top of each perievent histogram. b, Changes of the relative proportions of neurons responding to the auditory stimulus and/or reward for monkeys C and J.
Figure 7.
Changes of population responses of TANs during the learning of the stimulus–reward association. Histograms show, for one monkey, neuronal data from the four phases of training (left) and from separate blocks of trials in which the liquid reward was delivered alone (right). Data were taken from the same neurons tested in both the conditioning procedure and outside of the task, with the exception of the first and fourth periods. Vertical scale indicates mean impulse rate. N, Number of neurons included for each population histogram.
References
- Aosaki T, Graybiel AM, Kimura M ( 1994a) Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265: 412-415. - PubMed
- Aosaki T, Kimura M, Graybiel AM ( 1995) Temporal and spatial characteristics of tonically active neurons of the primate's striatum. J Neurophysiol 73: 1234-1252. - PubMed
- Apicella P, Ljungberg T, Scarnati E, Schultz W ( 1991) Responses to reward in monkey dorsal and ventral striatum. Exp Brain Res 85: 491-500. - PubMed
- Apicella P, Scarnati E, Ljungberg T, Schultz W ( 1992) Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J Neurophysiol 68: 945-960. - PubMed
Publication types
MeSH terms
LinkOut - more resources
Full Text Sources